[go: up one dir, main page]

Academia.eduAcademia.edu

The trade of medicinal animals in Brazil: current status and perspectives

2013, Biodiversity and Conservation

The trade of medicinal animals in Brazil: current status and perspectives Felipe S. Ferreira, Hugo FernandesFerreira, Nivaldo A. Léo Neto, Samuel V. Brito & Rômulo R. N. Alves Biodiversity and Conservation ISSN 0960-3115 Biodivers Conserv DOI 10.1007/s10531-013-0475-7 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be selfarchived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy Biodivers Conserv DOI 10.1007/s10531-013-0475-7 REVIEW PAPER The trade of medicinal animals in Brazil: current status and perspectives Felipe S. Ferreira • Hugo Fernandes-Ferreira • Nivaldo A. Léo Neto Samuel V. Brito • Rômulo R. N. Alves • Received: 16 May 2012 / Accepted: 20 March 2013 Ó Springer Science+Business Media Dordrecht 2013 Abstract In cities, the trade of medicinal products derived from animals, especially as raw materials, is concentrated in local and traditional markets. The lack of studies on commercialised medicinal faunas restricts an evaluation of the impact of this activity on the exploited species. Within this context, this work reviewed the literature on the trade of medicinal animals in local markets, focusing on urban zootherapy in Brazil and the social factors involved in these practices. Our results reveal that at least 131 species are sold for medicinal purposes in markets and open fairs in Brazil, but results obtained from statistical estimators suggest that this trade actually encompasses a greater richness of species. The medicinal animals sold in Brazil are used to treat 126 illnesses and/or symptoms. Despite the trade of wild animals, including species that are present on the list of endangered species, being forbidden in Brazil, it has been demonstrated that this activity remains common in some Brazilian cities, occurring illicitly and without due monitoring by competent environmental agencies. The results illustrate the need for further research, which should encompass a larger number of cities, especially in regions where information on this subject is currently lacking. Keywords Animal conservation  Ethnozoology  Traditional medicine  Wildlife trade  Zootherapy Introduction Urban centres are characterised by complex interactions of social, economic, cultural and environmental factors (Alberti 2005). The peculiarity of the urban centers helps preserve F. S. Ferreira (&)  H. Fernandes-Ferreira  N. A. Léo Neto  S. V. Brito Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Departamento de Sistemática e Ecologia, Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraı́ba (UFPB), Campus I, João Pessoa, PB 58051-900, Brazil e-mail: ferreira_fs@yahoo.com.br R. R. N. Alves Departamento de Biologia, Universidade Estadual da Paraı́ba, Campina Grande, PB, Brazil 123 Author's personal copy Biodivers Conserv traditions and knowledge regarding biodiversity, including its use for medicinal purposes (Ceuterick et al. 2008). The most commonly used products in traditional medicine come from animals and plants, and represent an important alternative to drugs from the pharmaceutical industry (Alves and Rosa 2005). In cities, the trade of medicinal products derived from plants and animals is concentrated in local markets or open fairs (Van den Berg 1984; Vázquez et al. 2006; Albuquerque et al. 2007a; Alves and Rosa 2010; Alves and Alves 2011). Local markets are considered to be important centres for gathering, concentrating, storing and spreading empirical knowledge concerning the therapeutic use of the local biodiversity thus favouring the resilience and maintenance of knowledge about these medicinal species (Monteiro et al. 2010; Alves et al. 2013). The importance of these public markets and open fairs is not restricted to the maintenance and development of knowledge concerning the use of the biological resources for medicinal purposes. Albuquerque et al. (2007a) claim that public markets, on a small scale, may also represent the biodiversity of a region, allowing identification of extensive exploitation areas and providing information that will assist monitoring of regional biodiversity. Despite its cultural, socio-economic and environmental importance, few researchers have investigated the trade of biological resources in public markets and/or open fairs (Jain 2000). In the last decade, however, some research has been undertaken on this theme, especially with regard to medicinal plant markets, which has received the attention of many ethnobotanists (Williams et al. 2000; Albuquerque et al. 2007a; Monteiro et al. 2010; Mati and de Boer 2011). Nevertheless, the trade of animals for medicinal purposes has been largely overlooked in the literature, with this sort of trade only recently being brought to the attention of researchers (Vázquez et al. 2006; Alves and Rosa 2007; Oliveira et al. 2010; Whiting et al. 2011; Ferreira et al. 2012; Ashwell and Walston 2008; Van and Tap 2008). The studies cited have revealed that extensive medicinal use of animal parts and products is sustained by a thriving trade in medicinal animals, conducted mainly by herbalists in markets (Alves et al. 2013). Connected to cultural and biological questions of animal trade, the socio-economic aspects are also essential to the maintenance of this activity. For salesmen (often known as herbalists, even if they also sell animal products) and suppliers (collectors and/or profiteers), the trade of medicinal animals represents an important source of income (Alves et al. 2008a). The lack of studies on traded medicinal faunas restricts an evaluation of the impact of this activity on the exploited species. As some authors recognise (Alves et al. 2007; Moura and Marques 2008), the exploitation of species for medicinal purposes may represent an additional pressure on wild fauna, although the influence of the medicinal use of these animals on the conservation of the involved species needs to be thoroughly investigated. Williams et al. (2007) stated that ethnobiological surveys carried out in public markets represent the first step towards the identification of priority species and the establishment of management plans. The trade of medicinal animals is routine practice in several countries around the world (Apaza et al. 2003; Soewu 2008; Whiting et al. 2011; Kang and Phipps 2003; Ashwell and Walston 2008, Alves et al. 2013). Due to the conservation status of many animal species sold for medicinal purposes (Alves and Rosa 2005; Alves 2008. Alves 2012), there are ecological, cultural, social and public health implications associated with their use (Alves et al. 2013). As a result of its faunal and cultural diversity, Brazil represents an excellent scenario for researching the trade of medicinal animals, a common practice in urban areas 123 Author's personal copy Biodivers Conserv of the country, which stand out as having a complex knowledge on the medicinal use of the fauna (Ferreira et al. 2012; Alves et al. 2009; Alves et al. 2013). Within this context, this work reviewed the literature on the trade of medicinal animals in local markets, focusing on urban zootherapy in Brazil and the social factors involved in these practices. The aims of this study were as follows: (i) to estimate the species richness of medicinal animals sold in Brazil; (ii) to evaluate the versatility of different animal species by calculating their relative importance value; (iii) to discuss the idea of utilitarian redundancy in the trade of animals in Brazil; (iv) to discuss those aspects that influence the choice of species for zootherapeutic product trading; and (v) argue about the conservation of species traded for medicinal purposes in Brazil. Materials and methods To examine the medicinal animal trade within Brazilian cities, we reviewed all the available references and reports on this topic. Information was gathered from published articles, books and book chapters, theses and dissertations, as well as from reports available in international online databases such as Science Direct (www.sciencedirect.com), Scirus (www.scirus.com), Google Scholar, Scopus (www.scopus.com), Web of Science (www.isiknowledge.com), and Biological Abstracts (science.thomsonreuters.com) using the following search terms:—medicinal animals ? trade ? Brazil—zootherapy ? commercialization ? Brazil, and—Wildlife trade ? Brazil. Information was compiled from 15 studies (undertaken between 1996 and 2012), which recorded the trade of medicinal fauna in 20 Brazilian cities (Fig. 1), from the following regions: Northeast (Crato, Juazeiro do Norte and Fortaleza [Ceará state]; João Pessoa and Campina Grande [Paraı́ba state]; São Luı́s [Maranhão state]; Teresina [Piauı́ state]; Recife, Caruaru and Santa Cruz do Capibaribe [Pernambuco state]; Maceió [Alagoas state]; Aracaju [Sergipe state]; Natal [Rio Grande do Norte state]; Feira de Santana and Salvador [Bahia state]); North (Belém [Pará state] and Boa Vista [Roraima state]); Midwest (Planaltina, Guará and Sobradinho [Distrito Federal state]) (Almeida and Albuquerque 2002; Silva et al. 2004; Alves and Rosa 2007, 2010; Alves et al. 2008a, 2009, 2010; Freire 1996; Oliveira et al. 2010; Costa-Neto 1999; Andrade and Costa-Neto 2006; Pinto and Maduro 2003; Ferreira et al. 2009a, 2012; Costa Neto and Motta 2010). Only taxa identified to the species level were considered. A database of commercialised medicinal species was created, including the animal parts used and the diseases and/or symptoms treated. Those diseases cited in revised studies were categorised according to the International Classification of Diseases model suggested by the World Health Organization (WHO 2012). The disease categories listed by the WHO does not consider emic diseases (as ‘‘attract money’’, simpatias, evil eyes, etc.), for that reason we included an ‘‘undefined illnesses’’ category, which includes all citations for diseases with unspecific symptoms. For each city where research on the trade of animals was undertaken, the following information was included: number of species identified, the species cited most often, the animal parts used most often and the biome surrounding the city. Estimate of species richness Data of the presence and absence (incidence data) of the species in the markets of Brazil were used to estimate the richness of medicinal species sold in each city. First, the data were divided into three groups (all animals, vertebrates [wild vertebrates and domestic 123 Author's personal copy Biodivers Conserv Fig. 1 Map demonstrating the locations of the studies examined in this work vertebrates] and invertebrates [marine invertebrates and terrestrial invertebrates]). Species richness was calculated utilizing the estimators based on incidence data, namely CHAO 2, ICE, Jackknife 1 and Jackknife 2. We decided to use these four estimators because they 123 Author's personal copy Biodivers Conserv utilized different methods for determining species richness (see Colwell and Coddington 1994). Jacknife 1 and 2, Chao 2 and ICE have been utilised in ethnobotanical and ethnozoological studies (Begossi 1996; Williams et al. 2000, 2007; Whiting et al. 2011; Ferreira et al. 2012). Species richness was calculated using the Estimate S 8.2.0 program (Colwell 2009). Coefficient of similarity The composition of the species cited was compared between the cities studied by means the similarity index based on data of multiple incidence. The similarity between the localities was estimated using the distance coefficient of Jaccard (see Chao et al. 2005). The similarity matrix was constructed and grouping analysis performed in the Past program (Hammer et al. 2001). Relative importance (RI) The RI of the species cited was calculated (Bennett and Prance 2000). This index is used to measure the importance of a species on the basis of its versatility, assuming that the potential utility of a species is associated with the number of attributed uses (see Albuquerque et al. 2006, 2007b). RI was calculated according to the following formula: RI ¼ NCS þ NP; where NCS is categories of diseases treated by a species (e.g., diseases of the respiratory system, diseases of the musculoskeletal system and connective tissue, etc.), while NP is number of diseases treated by a specie (e.g., sore throat, asthma, rheumatism, etc.). NCS is obtained by the relationship between the number of categories of diseases treated by a given species (NCSS) divided by the total number of number of categories of diseases treated by the most versatile species (NCSSV). NP is obtained by the relationship between the number of diseases treated attributed to a species (NPS) divided by the number of diseases treated attributed to the most versatile species (NPSV). The most versatile species are those that have the greatest number of medicinal properties. Utilitarian redundancy of diseases and/or symptoms Utilitarian redundancy of zootherapeutic products was tested according to the model adapted from Albuquerque and Oliveira (2007). According to these authors, the idea of utilitarian redundancy is based on the theory of ecological redundancy (this theory indicates that all species presents specific functions in the ecosystem, but some ones can show similar functions, minimizing damages in the ecosystem due the extinction [see Wellnitz and Poff 2001; Scarff and Bradley 2002]). Therefore, the notion of functional redundancy relies on the presumption that some species are utilized for the treatment of more than one disease and/or symptom, such that the inclusion of more than one species within a disease category can be a mechanism of reducing the impact on the animals sold for medicinal purposes. To evaluate this hypothesis, diseases were categorized according to the levels of redundancy proposed by Albuquerque and Oliveira (2007): highly redundant (C15 % of the number of species utilized), redundant (15 % \the number of species C5 %) and not very redundant (\5 % of the species). 123 Author's personal copy Biodivers Conserv The conservation status of animal species To discuss the conservation of animals traded for medicinal purposes, the conservation status of all the recorded species was obtained from IUCN (2011) according version 3.1 (http:// www.iucnredlist.org) and also from the database of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES 2012) (CITES; http://www.cites.org). Alternatives to the wildlife trade Based on the definition of relative importance, (see Bennett and Prance, 2000; Silva et al. 2010), any significant differences between the RI values of wild and domestic species were determined, to assess alternatives to the use of wild species. Differences in the RI of the two groups of animals (wild and domestic species) were compared using the Kruskal– Wallis test (Sokal and Rholf 1995). Results and discussion Species richness traded The reviewed data reveal that at least 131 species are sold for medicinal purposes in markets and open fairs in Brazil (Table 1; Fig. 2). These species were recorded for 20 cities, a small sampling considering that there are 5,570 cities in Brazil (IBGE 2012). The results obtained using statistical estimators (ICE, Chao 2 and Jackknife 1 and 2) suggest that this trade actually encompasses a greater richness of species of the sites sampled. The predicted number of species involved varied from 172 to 200, depending on the estimator (Table 2). According to Alves (2010), the limited number of studies involving markets and open fairs may be related to the clandestine or semi-clandestine character of the activity of trading wild animals in Brazil, which makes it difficult to obtain access to these activities. Given this situation, the use of species richness estimators represents an important tool for calculating the probable number of medicinal species sold in urban areas of Brazil. Considering the species recorded, the taxonomic groups most representative were: mammals with 36 species (29 wild and 7 domestic) and reptiles with 31 species (Fig. 3). Currently, at least 701 species of mammals and 738 of reptiles are known for Brazil (Paglia et al. 2012; Bérnils and Costa, 2012), which means that 4.13 % of the mammalian species and 4.2 % of the reptilian species in Brazil are marketed for medicinal purposes. We see that the number of species sold for medicinal purposes is not related to the quantity of species available in Brazil, since taxa with greater species richness in Brazil, such as birds (1,830 species), fishes (3,890 species) and insects (90,300 species) (Comitê Brasileiro de Registros Ornitológicos, 2011; Menezes et al. 2003; Buckup et al. 2007; Rafael et al. 2009), showed fewer species sold as medicinal products (15 bird species; 0.4 % of the Brazilian avifauna); fishes (16 species; 0.4 % of the Brazilian ichthyofauna) and insects (16 species; 0.01 % of the Brazilian entomofauna), fewer than mammals and reptiles. Among the 131 species of animals sold in Brazil, there is a predominance of vertebrates (n = 101), following a tendency reported in several places in Latin America (Alves and Alves 2011) and also in some countries in Africa (El-Kamali 2000; Sodeinde and Soewu 1999; Whiting et al. 2011) and Asia (Ashwell and Walston 2008; Van and Tap 2008). On a global scale, available data on the trade of medicinal animals are scarce and limited. Examples include research by El-Kamali (2000), who reported the trade of 23 animal 123 Class/family/species/local name RI Part used Cities References 0.10 Whole animal Be 1 0.10 Shell As 2 0.20 Shell Ar; Sa 2 0.10 Shell Sa 2 0.10 Flesh and shell SL 1 0.10 Shell Be; SL 1 0.20 Whole animal Re 3 Cnidarians Class Hydrozoa Physaliidae Physalia physalis, Portuguese-man-of-war, caravela Biodivers Conserv Table 1 Animal species commercialized for medicinal purposes in Brazil Molluscs Class Gastropoda Achatina fulica, Giant east African snail, caramujo gigante africano Strombidae Strombus pugilis, West Indian fighting conch, estrombo-lutador- das-Índias-Ocidentais Class Bivalvia Cardiidae Trachycardium muricatum, Yellow prickly cockle, rala-côco Mytilidae Mytella guyanensis, Mussel, sururu Ostreidae Crassostrea rhizophorae, Mangrove oyster, ostra do mangue Crustaceans Calappidae 123 Malacostraca Calappa ocellata, Ocellate box crab, caranguejo-gojá Author's personal copy Achatinidade 123 Table 1 continued Class/family/species/local name RI Part used Cities References 0.10 Whole animal FS 4 Apis mellifera, Honey bee, abelha italiana 0.98 Honey and wax Ar; Fo; Ma; Re; Sa; Cra; JN; CG; Ca; SCC; Te; Na; SL; Be 1; 2; 5; 6; 7; 8; 9 Frieseomelitta varia, Bee, abelha moça branca 0.10 Honey SCC 8 Melipona compressipes, Stingless bee, tiúba 0.43 Honey Te; SL; Be 1 Melipona scutellaris, Stingless bee, uruçú 1.18 Honey and wax Ma; Re; Cra; JN; CG; Ca; SCC; Na; SL; Be 1; 2; 5; 6; 7; 9; 10 Melipona subnitida, Stingless bee, jandaı́ra 0.55 Honey and wax Fo; Cra; J N; CG; Na; SL 1; 2; 5; 6; 9 Partamona cupira, Stingless bee, cupira 0.75 Honey and wax Fo; Ma; Re; Cra; JN; SCC 2; 5; 8 Tetragonisca angustula, Stingless bee, abelha mosquito 0.13 Honey Na; Be; SCC 1; 8; 9 Trigona spinipes, Stingless bee, arapuá 0.25 Honey and wax Na; Be, FS 1; 4; 9 0.30 Viscera, wings and whole animal Ar; Cra; JN; Ca; SCC 2; 5; 7; 8 0.10 Whole animal CG; JP 1; 6 0.20 Whole animal CG; JN 5; 6 0.10 Leg Cra; JN 5 Squillidae Cloridopsis dubia, Mud mantis, barata-do-mar Insects Class Insecta Apidae Author's personal copy Blattidae Periplaneta americana, Cockroach, barata Chrysomelidae Coraliomela brunnea, Fake cockroach, barata de coqueiro Dinoponera quadriceps, Bullet ant, trinca-cunhão Gryllidae Gryllus assimilis, Cricket, grilo Muscidae Biodivers Conserv Formicidae Class/family/species/local name Musca domestica, House fly, mosca RI Part used Cities References 0.10 Whole animal SCC 8 0.13 Whole animal Br 11 Tenebrionidae Palembus dermestoides, peanut beetle, besouro-do-amendoim, Biodivers Conserv Table 1 continued Termitidae 0.17 Whole animal Fo 2 0.13 Whole animal Ca; SCC 7; 8 Echinaster brasiliensis, Sea star, estrela-do-mar 0.20 Whole animal Re; Ca; FS 3; 4; 7 Echinaster echinophorus, Sea star, estrela-do-mar 0.66 Whole animal Ar; Ma; Sa; Ca 2; 7 0.63 Whole animal Ar; Fo; Ma; Re; Sa; JN; JP; CG; Ca; SCC; Na; Te; SL; Be 1; 2; 6; 7; 8; 9 0.20 Whole animal JP; CG; Ca 1; 6; 7; 10 0.10 Whole animal Ca; Re 3; 7 0.10 Whole animal Ca 7 Echinoderms Class Asteroidea Echinasteridae Oreasteridae Oreaster reticulatus, Sea star, estrela do mar Luidiidae Luidia senegalensis, Sea star, estrela-do-mar Class Echinoidea Echinometridae Echinometra lucunter, Rock boring urchin, ouriço-do-mar Mellitidae 123 Mellita quinquiesperforata, Sand dollar, bolacha-de-praia Fishes Class Actinopterygii Author's personal copy Nasutitermes corniger, Termite, cupim Nasutitermes macrocephalus, Termite, cupim de aroeira 123 Table 1 continued Class/family/species/local name RI Part used Cities References 0.10 Fat Cra; JN 5 0.20 Skin SL 1 1.06 Fat Ar; Fo; Cra; CG; SCC; Te; FS; Na 1; 2; 4; 6; 8; 9 1.37 Fat Ar; Fo; Ma; Re; Sa; JN; Ca; SCC; SL; Te; FS; Na; Be; BV; Br 1; 2; 4; 5; 7; 8; 9; 11; 12 0.10 Scale SL; Be 1 0.10 Scale Be 1 0.13 Fat BV 12 Cynoscion acoupa, Acoupa weakfish, pescada amarela, LC 0.13 Otolith SL 1 Cynoscion leiarchus, Smooth weakfish, pescada branca 0.13 Otolith SL 1 1.05 Whole animal Ar; Fo; Ma; Re; Sa; JN; JP; CG; Ca; SCC; SL; Te; FS; Na; Be 1; 2; 4; 6; 7 Anostomidae Leporinus steindachneri, Black piau, piau Balistidae Balistes vetula, Queen triggerfish, cangulo, VU* Erythrinidae Hoplias malabaricus, Trahira, traı́ra Electrophorus electricus, Electric eel, peixe elétrico, LC Author's personal copy Gymnotidae Megalopidae Megalops atlanticus, Tarpon, camurupim Osteoglossidae Arapaima gigas, Giant arapaima, pirarucu, DD*, II Pimelodidae Phractocephalus hemioliopterus, Redtail Catfish, pirarara Sciaenidae Hippocampus reidi, Longsnout seahorse, cavalo marinho DD, II Prochilodontidae Biodivers Conserv Syngnathidae Class/family/species/local name RI Part used Cities References 0.10 Fat Cra; JN 5 0.10 Fat FS 4 Carcharhinus limbatus, Blackfin shark, sucuri preto NT 0.10 Cartilage SL 1 Carcharhinus leucas, Cub shark, tubarão, NT – – Ca 10 Pristis pectinata, Sawfish, Smalltooth sawfish, espadarte CR, I 0.23 Rostral expansion Be 1 Pristis perotteti, Largetooth sawfish, espadarte, CR, I 0.23 Rostral expansion Be 1 0.98 Secretions, fat and skin Ar; Fo; Re; Sa; SCC 2; 8 Leptodactylus labyrinthicus, South American pepper frog, rã-pimenta, LC 0.15 Fat Fo 2 Leptodactylus vastus, Northeastern pepper frog, rã-pimenta, LC 0.28 Fat Fo 2 Prochilodus nigricans, Black prochilodus, curimatã Tetraodontidae Sphoeroides testudineus, Checkered puffer, baiacu Biodivers Conserv Table 1 continued Class Elasmobranchii Carcharhinidae Amphibians Class Amphibia Bufonidae Rhinella jimi Cururu toad, sapo cururu, LC Leptodactylidae Reptiles 123 Class Reptilia Cheloniidae Author's personal copy Pristidae 123 Table 1 continued Class/family/species/local name RI Part used Cities References 1.01 Fat and carapace Fo; Sa 2 Phrynops geoffroanus, Geoffroy’s side-necked turtle, cágado 0.93 Carapace and fat JP; CG; Ca; SCC; SL; Na 1; 6; 7; 8; 9 Phrynops tuberosus, Cotinga river toadhead turtle, cágado 0.30 Carapace and fat Cra; JN 5 Mesoclemmys tuberculatus, Tuberculate toadhead turtle, cágado d’água 0.10 Carapace Ma 13 Chelonoidis denticulata, Yellow-footed tortoise, jabuti VU*, II 0.58 Carapace, fat, liver, urine and whole animal Ca; SCC; Be 1; 7; 8 Chelonoidis carbonaria, Red-footed tortoise, jabuti do pé vermelho, II 0.71 Carapace, fat, liver and blood Ca; SL; FS; Be 1; 4; 7 0.58 Fat Be; BV 1; 12 Caiman crocodilus, Common caiman, jacaré-tinga LR*, II 0.86 Skin, fat and tooth Cra; JP; CG; Ca; SL; Te; Be; BV 1; 5; 6; 7; 12 Caiman latirostris, Broad-snouted caiman, jacaré do papo-amarelo LR*, II 0.96 Skin, fresh, fat, leather and tooth JP; CG; Ca; SCC; SL; Te; Ma; FS; Na 1; 4; 6; 8; 9; 10; 13 Paleosuchus palpebrosus, Dwarf caiman, jacaré coroa LR*, II 0.48 Skin, fresh, fat and penis JP; CG; SL; Te; Be 1; 6 Melanosuchus niger, Black caiman, jacare açú, II 0.58 Fat, skin and penis Be 1 1.53 Fat, bone, feces and skin Ar; Fo; Ma; Sa; JP; CG; SL; Be; BV; Br 1; 2; 6; 11; 12; 14 Chelonia mydas, Green sea turtle, tartaruga verde, EN, II Chelidae Author's personal copy Testudinidae Podocnemididae Podocnemis expansa, Amazon river turtle, tartaruga da amazônia LR*, II Alligatoridae Boa constrictor constrictor, Common boa, jibóia, II Biodivers Conserv Boidae Class/family/species/local name Corallus caninus, Emerald tree boa, cobra papagaio, II RI Part used Cities References 0.10 Whole animal SL 1 Epicrates cenchria, Rainbow boa, salamanta, II 0.50 Fat and whole animal Fo; CG; Ca; Ma; FS 2; 6; 10; 13 Eunectes murinus, Anaconda, Green anaconda, sucuri, II 0.66 Fat Ca; SL Te; Be; BV 1; 7; 12 0.20 Whole animal, fat and skin CG; Ma 1; 6; 13 Biodivers Conserv Table 1 continued Colubridae Leptophis ahetula, Parrot snake, cobra cipó 0.10 Whole animal SL 1 Mastigodryas bifossatus, Rio tropical racer, jaracuçu 0.10 Whole animal Ma 13 Philhodryas olfersii, Lichtenstein’s green racer, cobra verde 0.10 Whole animal Sa 2 Spilotes pullatus, yellow rat snake, caninana 0.33 Bone, fat and whole animal Sa; Be 1; 2 Crotalus durissus, rattlesnake, cascavel LC, II 1.80 Fat, rattle, bone and skin Ar; Fo; Ma; Re; Sa; Cra; JN; JP; CG; Re; Ca; SCC; SL; Te; Ma; FS; Na; Be; BV; Br 1; 2; 3; 4; 5; 6; 7; 8; 9; 11; 12; 13; 14 Lachesis muta, Bushmaster, surucucu pico de jaca 0.23 Fat Ma; Be 1; 13 0.50 Fat and skin Ma 2; 13 0.75 Fat, bone and tail Ma; Re; CG; Ca; SCC; SL; Na; Be 1; 2; 6; 8; 9; 10 0.10 Whole animal CG 1 Viperidae Elapidae Micrurus ibiboboca, Caatinga coral snake, coral verdadeira Iguanidae 123 Iguana iguana, Common green iguana camaleão, II Gekkonidae Hemidactylus mabouia, House gecko, lagartixa Teiidae Author's personal copy Oxyrhopus trigeminus, Brazilian false coral snake, falsa coral 123 Table 1 continued Class/family/species/local name RI Part used Cities References 13 Ameiva ameiva, Giant ameiva, calango bico doce 0.10 Whole animal Ma Cnemidophorus ocelifer, Spix’s whiptail calango 0.35 Whole animal Ma 1; 13 Tupinambis merianae, Teju lizard, tiú LC, II 1.62 Fat, skin and tail Ar; Fo; Ma; Re; Sa; Cra; JN; JP; CG; Ca; SCC; Te; Na 1; 2; 5; 6; 7; 8; 9 Tupinambis teguixin, Teju lizard, tejuaçú, II 0.91 Fat, tail, skin, eggs, meat and bone SL; Be; Ma 1; 13 Tropiduridae 0.38 Whole animal, liver and fat Cra; JP; CG; Ma 1; 5; 6; 13 Tropidurus semiteniatus, Lizard, lagartixa 0.15 Whole animal CG 6 Author's personal copy Tropidurus hispidus, Lizard, lagartixa Birds Class Aves Anatidae Anas platyrhynchos, Mallard, pata, LC 0.35 Fat and eggs Sa; SCC 2; 8 Anser anser, Greylag goose, ganso, LC 0.15 Fat Re 2 Coragyps atratus, Black vulture, urubu, LC 0.45 Feather, liver, beak and fat Fo; Ma; Re; JN; JP; Ca; SCC; SL; Te; Be 1; 2; 6; 7; 8 Cyanocorax cyanopogon, White-naped jay, cancão, LC 0.10 Whole animal SCC 8 0.17 Fat Sa 2 0.10 Whole animal and fresh Cra; SL 1; 5 0.10 Fat BV 12 Cathartidae Columbidae Columba livia, Rock pigeon, pombo, LC Cuculidae Pipridae Pipra aureola, Crimson-hooded manakin, uirapuru, LC Phasianidae Biodivers Conserv Crotophaga ani, Smooth-billed ani, anu, LC Class/family/species/local name Part used Cities References Gallus gallus, Chicken, galinha, LC 1.46 Fat, spur and gizzard Ar; Fo; Re; Sa; Cra; JN; JP; CG; Ca; SCC; SL; Te; FS; Na; Be; BV; Br 1; 2; 4; 5; 6; 7; 8; 9; 10; 11; 12 Pavo cristatus, Common peafowl, pavão, LC 0.53 Feather and fat Sa; Cra; Ca; SCC; FS; Ma 2; 5; 8; 10; 14 Numida meleagris, Helmeted guineafowl, Guiné, LC 0.40 Fat and blood Sa; Ca; SCC; Br 2; 6; 8; 11 Meleagris gallopavo, Wild turkey, peru, LC 0.87 Feather Ca 8 0.10 Beak Be 1 0.58 Fat and skin Re; JP; CG; Ca; FS; Na; Be; Br 1; 2; 6; 7; 10; 14 0.10 Eggs shells SCC 8 0.10 Feather SCC 8 0.58 Fat, penis and bile Sa; SL; Be; BV; Br 1; 2; 12; 13 Bos taurus, Cow, boi 1.13 Fat, tail, skin, urine, penis, horn and bile Fo; Ma; Re; Sa; C; JN; Ca; SCC; SL; Te; FS; Br; BV 1; 2; 3; 5; 10; 3; 14; 8; 7; 11; 12 Ovis aries, Sheep, carneiro 1.14 Fat, horn and suet Ar; Fo; Ma; Re; Sa; Cra; JP; Re; Ca; SCC; SL; Na; Be; BV; Br 1; 2; 3; 5; 6; 7; 8; 9; 10; 12 Ramphastidae Ramphastos tucanus, White-throated toucan, tucano, LC, II Rheidae Rhea americana, Greater rhea, ema, NT, II Struthionidae Struthio camelus, Common ostrich, avestruz, LC Tinamidae Nothura maculosa cearensis, Spotted nothura, codorniz Mammals Class Mammalia Agoutidae Cuniculus paca, Spotted paca, paca, LC, III Bovidae Author's personal copy RI Biodivers Conserv Table 1 continued 123 123 Table 1 continued Class/family/species/local name RI Part used Cities References Bubalus bubalis, Water buffalo, bufalo 0.45 Horn, fat and tail SL; Re 1; 2 Capra hircus, Domestic goat, bode 0.93 Horn, fat and brain SL; Ar; Ma; Re; Sa 1; 2 0.20 Skin, claw and bones Ca; Be, CG 1; 6; 7; 10 Cerdocyon thous, Crab-eating fox, raposa LC, II 0.88 Fat Ma; Re; Cr; JN; SCC; Te; Na, CG 2; 5; 6; 8; 9 Canis lupus, Domestic dog, cachorro, LC 0.10 Fat Fo 2 0.13 Fat and manure SCC 8 Mazama gouazoubira, Gray brocket, veado catingueiro, LC 0.38 Tail, horn, nail and tibia FS; Fo; Ma; Re; Sa 2; 4 Mazama americana, Red brocket, veado gaeado, DD 0.10 Tibia CG; Ca 6; 10 0.35 Penis, bone and fat Be 1 Dasypus novemcinctus, Nine-banded armadillo, tatu galinha, LC 1.06 Fat, tail, leg and skin Ma; Re; Cr; JN; Ca; SL 1; 2; 5; 7 Euphractus sexcinctus, Six-banded armadillo, tatu peba, LC 1.33 Legs, tail, urine, skin and fat Ma; Re; Sa; Cr; JN; JP; Ca; SCC; SL; Na 1; 2; 5; 7; 8; 9 Didelphis marsupialis, Common opossum, mucura, LC 0.25 Fat SL; Be 1 Didelphis albiventris, White-eared opossum, timbu, LC 0.20 Bone Ca; Na, CG 6; 7; 9 Bradypodidae Bradypus variegatus, Brown-throated three-toed sloth, preguiça LC, II Canidae Author's personal copy Caviidae Kerodon rupestris, Rock cavy, mocó, LC Cervidae Cebidae Cebus apella, Brow capuchin, macaco-prego, LC, II Dasyponidae Biodivers Conserv Didelphidae Class/family/species/local name RI Part used Cities References 0.33 Milk and hoof Ca; SCC; SL 1; 7; 8 Coendou prehensilis, Brazilian porcupine, porco espinho, LC 0.93 Spines Ar; Ma; Re; Sa; JP; CG; Re; Ca; SCC; SL; Te; FS; Be 1; 2; 3; 4; 6; 7; 8 Coendou bicolor, bicolored-spined porcupine, porco espinho, LC – – Ca 10 0.30 Eyes Re; Ca 2; 10 0.63 Bone, fat and fresh SL; Te; BV; Br 1; 11; 12 0.35 Bone, fat and meat Ca; SCC 7; 8 0.10 Skin Sa 2 Procyon cancrivorus, Crab-eating raccoon, guaxinim LC 0.61 Fat and skin JN; SL; Te 1; 5 Nasua nasua, South American coati, quati, LC, III 0.33 Fat and penis FS; Be 1; 4; 14 0.23 Navel and fat Cra; Re 2; 5 0.40 Fat and paw Be; BV 1; 12 Equidae Equus asinus, Asino, jumento Biodivers Conserv Table 1 continued Erethizontidae Leopardus pardalis, Ocelot, gato maracajá, LC, II Hydrochoeridae Hydrochoerus hydrochaeris, Capybara, capivara, LC Mustelidae Conepatus semistriatus, Striped hog-nosed skunk gambambá, LC Mymercophagidae Myrmecophaga tridactyla, Giant anteater. tamanduá bandeira, VU, II Procyonidae Suidae Sus scrofa, pig, porco, LC 123 Tapiridae Tapirus terrestris, South American tapir, anta, VU, II Author's personal copy Felidae 123 Table 1 continued Class/family/species/local name RI Part used Cities References 0.13 Fat SL 1 0.30 Whole animal Sa 2 Tayassuidae Pecari tajacu, Collared peccary, caititu, LC, II Phyllostomidae Desmodus rotundus, Vampire bat, morcego, LC Delphinidae 0.73 Fat and penis SL; Be; BV 1; 12 Sotalia guianensis, Guianan river dolphin, boto DD, I 1.73 Fat, penis, eyes and blood Ar; Fo; Ma; Re; Sa; SL; Be 1; 2 0.48 Fat Be 1 Trichechus inunguis, Amazon manatee, peixe-boi VU, I 0.75 Fat and skin JP; Ca; SL; FS; Be 1; 4; 7 Trichechus manatus, Manatee, peixe-boi VU, I 1.80 Fat and skin Ar; Ma; Re; Sa; JP; SL; Te; Be; FS 1; 2; 4 0.10 Fat JP; SL; Be 1 0.10 Fat JP; SL; Be 1 Author's personal copy Sotalia fluviatilis, Gray dolphin, boto DD, I Iniidae Inia geoffrensis, Amazon river dolphin, boto rosa DD, II Trichechidae Balaenopteridae Balaenoptera acutorostrata, Common minke whale, baleia minke, LC, I Physeteridae Physeter macrocephalus, Sperm whale, cachalote, VU Cities: BV Boa Vista, Be Belém, FS Feira de Santana, JP João Pessoa, CG Campina Grande, Na Natal, Te Teresina, Ca Caruaru, SCC Santa Cruz do Capibaribe, JN Juazeiro do Norte, Cra Crato, RE Recife, BR Distrito Federal, SL São Luiz, Ma Maceió, Fo Fortaleza, Ar Aracaju, Sa Salvador References: 1 = Alves and Rosa (2007), 2 = Ferreira et al. (2012), 3 = Silva et al. (2004), 4 = Costa-Neto (1999), 5 = Ferreira et al. (2009a), 6 = Alves et al. (2010), 7 = Alves et al. (2009), 8 = Alves et al. (2008a, b, c), 9 = Oliveira et al. (2010), 10 = Almeida and Albuquerque (2002), 11 = Costa Neto and Motta (2010), 12 = Pinto and Maduro (2003), 13 = Freire (1996), 14 = Andrade and Costa-Neto (2006) Biodivers Conserv Categories of IUCN Red List according to version 3.1: DD data deficient, LC least concern, NT near threatened, VU vulnerable, EN endangered, CR critically endangered, VU* vulnerable and LR* lower risk according to version 2.3, Categories of CITES Appendix I, II and III Author's personal copy Biodivers Conserv Fig. 2 Examples of animals used as medicine that are sold in public markets in Brazil. a Crotalus durissus, b Tupinambis merianae c Caiman crocodilus, d Caiman latirostris, e Boa constrictor, f Coragyps atratus, g Euphractus sexcintus, h Coendou prehensilis (Photos: a, b Daniel Loebmann, c Igor Joventino Roberto, d Marco Antonio de Freitas, e Carlos Candido, f–h Hugo Fernandes-Ferreira) 123 Author's personal copy Biodivers Conserv Table 2 Estimators of species richness showing the number of species that may be marketed in Brazil All animals Sobs ICE Chao 2 Jack 1 Jack 2 131 193 172 178 200 Wild vertebrate 87 132 120 120 137 Domestic vertebrate 14 17 15 17 18 Marine invertebrate 14 21 18 20 24 Terrestrial invertebrate 16 19 16 19 19 Fig. 3 Number of animal species used as remedies per taxonomic category in Brazil species for therapeutic purposes in Sudan; Sodeinde and Soewu (1999), who described 45 species sold in markets in Nigeria; and Ashwell and Walston (2008), who reported the use and trade of 43 species of medicinal animals in Cambodia. As expected, the number of species of medicinal animals sold in Brazilian public markets (n = 131) is less than the number of medicinal plants, according to a review carried out by Monteiro et al. (2010), which listed 265 species of medicinal plants (varying between 28 and 265 species) sold in the markets of 15 Brazilian cities. Analysing each Brazilian city where the trade of zootherapeutic products was investigated, and only taking into consideration the identified species, we discovered that the number of commercialised animal species varied from 11 to 48 (Table 3). As far as Almeida and Albuquerque (2002) are concerned, the differences in the number of animal and plant species marketed can be explained by the greater tradition in the use of medicinal plants in markets and open fairs, suggesting that vendors probably have a greater and more consistent knowledge base of plants compared to medicinal animals. Another factor that can lead to a relatively lower availability of medicinal animal species in the markets is the illegality of their sale when the products are derived from wild animals (Alves and Rosa 2010). The vendors generally sell both medicinal plants and animals in the markets, but the majority do not admit to handling products from wild animals, because they are aware that it is prohibited (Alves et al. 2013). Parts of animals used Although whole animals are traded, most of the time the zootherapeutic products sold are body parts or metabolic secretions, including the following: fat (derived from 51 % of animals), whole animal (26 % of animals), skins (17 % of animals) and bones (8 % of animals) (Fig. 4; Table 1). Of the parts used, fat is the most traded product in all cities, and 123 Author's personal copy Biodivers Conserv Table 3 Overview of trade in medicinal animals in Brazil Cities Number of species Species most cited Biome in which the city is located References Crato 22 Phrynops tuberosus Caatinga Ferreira et al. (2009a) Juazeiro do Norte 22 Tupinambis merianae Caatinga Ferreira et al. (2009a) Fortaleza 24 Apis mellifera Caatinga Ferreira et al. (2012) João Pessoa 19 Hippocampus reidi; Paleosuchus palpebrosus; Caiman crocodilus Atlantic forest Alves and Rosa (2007, 2010) Campina Grande 32 Gallus gallus Caatinga Alves et al. (2010) Recife 27 Ovis aries Atlantic forest Silva et al. (2004) and Ferreira et al. (2012) Caruaru 34 Oreaster reticulatus; Hippocampus reidi; Caiman crocodilus Caatinga Almeida and Albuquerque (2002) and Alves et al. (2009) São Luiz 47 Boa constrictor Amazon Forest Alves and Rosa (2007, 2010) Teresina 22 Crotalus durissus Caatinga Alves and Rosa (2007, 2010) Santa Cruz do Capibaribe 35 Crotalus durissus; Gallus gallus Caatinga Alves et al. (2008a) Aracaju 18 Echinaster echinophorus Atlantic Forest Ferreira et al. (2012) Maceió 25 Sotalia guianensis Atlantic Forest Freire (1996) and Ferreira et al. (2012) Natal 19 Tupinambis merianae; Cerdocyon thous Atlantic Forest Oliveira et al. (2010) Salvador 31 Hipocampos reidi Atlantic Forest Ferreira et al. (2012) Feira de Santana 16 – Caatinga Costa-Neto (1999) and Andrade and Costa-Neto (2006) Belém 45 Hippocampus reidi Amazon Forest Alves and Rosa (2007, 2010) Boa Vista 15 – Amazon Forest Pinto and Maduro (2003) Planaltina, Guará and Sobradinho 11 Crotalus durissus Cerrado Costa Neto and Motta (2010) the prominent use of fat for medicinal purposes may be attributed to the fact that the main animals used are vertebrates, which provide large amounts of body fat (Alves et al. 2008a). In fact, most of the registered medicinal vertebrates (66 species) have their fat sold for medicinal purposes. Diseases and/or symptoms treated by zootherapeutic products According to the data compiled here, medicinal animals sold in Brazil are used to treat 126 illnesses and/or symptoms. The illnesses and/or symptoms treated with commercialised zootherapeutic products can be divided into 15 categories (Table 4). The categories treated 123 Author's personal copy Biodivers Conserv Fig. 4 Examples of animal products used as remedies that are sold. a Dried starfish (Oreaster reticulatus), b liver powder of Coragyps atratus, c dried seahorses (Hippocampus reidi), d horn of Bos taurus, e hoof of Mazama gouazoubira, f carapace of Phrynops tuberosus, g secretions, fats, oils and honey of medicinal animals (Photos: Samuel C. Ribeiro) using the greatest number of species are: diseases of the respiratory system (72 species), undefined diseases (53 species) and diseases of the musculoskeletal system and connective tissue (48 species). The categories cited of illnesses are also frequently treated with medicinal animals in several other countries (Lev and Amar 2000, 2002; Vázquez et al. 2006; Mahawar and Jaroli 2008; Soewu 2008). Distribution of the medicinal animals per locality In analyzing the distribution of the animals per locality, we found that 16 species (12. 2 %) were cited for more than nine cities. The species most cited are: Crotalus durissus 123 Author's personal copy Biodivers Conserv Table 4 Categories of diseases treated with animal-based medicines that are sold in public markets in Brazil Categories Number of medicinal animals Diseases of the respiratory system 72 Undefined illnesses 53 Diseases of the musculoskeletal system and connective tissue 48 Diseases of the circulatory system 33 Infections and parasitic diseases 27 Diseases of the nervous system 23 Diseases of the digestive system 17 Diseases of the skin and the subcutaneous tissue 16 Diseases of the ear 12 Diseases of the urogenital system 11 Lesions caused by poisoning and other external causes 11 Neoplasias (tumours) 10 Mental and behavioural disturbances 2 Disorders of the immune system 2 Ophthalmological diseases 2 (rattlesnake), cited for 18 cities; Gallus gallus (chicken) cited in 17 cities; and Hippocampus reidi (longsnout seahorse), Electrophorus electricus (electric eel) and Ovis aries (sheep), which were cited for 15 cities. The greater incidence of some species can be associated with factors such as: (i) being a species of high cultural value for the users and (ii) the high availability of these species in the biomes in which the cities are located (Alves et al. 2013; Ferreira et al. 2012). The recording of species in only one locality (n = 50, 38 %) can be associated with the specificity of citations of use, the local preferences or low availability in the biomes around the cities where they are sold. Relative importance Among the recorded species, 90 (68.7 %) were cited for the treatment of more than one disease and/or symptom, therefore indicating their versatility. The most versatile species, in other words those with the highest RI values, were Trichechus manatus (manatee; RI = 1.8), Crotalus durissus (rattlesnake; RI = 1.8), Sotalia guianensis (Guianan river dolphin; RI = 1.73) and Tupinambis merianae (teju lizard; RI = 1.62). According to the high values of RI, probably, these four species have the highest the utilitarian value among species commercialized in Brazil. The RI determines the versatility of a species based on the number of attributed uses (Bennett and Prance 2000). High RI values suggest that the knowledge of a species is widely disseminated in a locality. In our review, we see that the species that showed the highest RI values have a more widespread use among the cities sampled, probably reflecting their utility for treating a greater diversity of diseases. In a broader context, indices such as RI are based on the consensus of informants (Silva et al. 2010), which assumes that a species is more culturally important the more knowledge about it is shared. 123 Author's personal copy Biodivers Conserv Utilitarian redundancy The data revised here, revealed that a single disease and/or symptom may be treated by more than one species, corroborating to the idea of utilitarian redundancy suggested by Albuquerque and Oliveira (2007). As shown in Fig. 5, the ‘highly redundant’ category encompasses 108 species, while in the ‘redundant’ and ‘not very redundant’ categories the number is significantly smaller (71 and 74, respectively). Based upon the model of utilitarian redundancy (Albuquerque and Oliveira 2007), the pressure exerted on animal species sold in the evaluated markets is probably small, such that most of species fall into the ‘highly redundant’ category, since they have several therapeutic alternatives. Consequently, conservation strategies should prioritise those species included in the ‘not very redundant’ category, since, based upon the redundancy model, the species included in this category have few equivalents for medicinal use. However, Albuquerque and Oliveira (2007) believe that some considerations must be taken when basing conservation strategies on the model tested here: (i) the idea of redundancy may be associated with the resilience of the local medical system, in other words, highly redundant categories would initially be more resilient than those with low redundancy; and (ii) even species categorised as redundant could have lower resilience if local users exhibit a greater preference for their products. Aspects that influence the choice of medicinal species Understanding the mechanisms that determine which species are traditionally sold in markets and fairs are essential to discussions regarding the conservation of Brazilian medicinal animals. Probably, the choice of animal species for trading in Brazil is a response to the interaction of biological (faunal composition of biomes around urban centers), cultural (traditions, beliefs and myths) and social (alternatives to allopathic drugs) features of the consumer population. The reviewed data showed that the cities where the research was done are located in the following biomes: Caatinga (eight cities), Atlantic Forest (six cities), Cerrado (three cities, covered by a single study) and Amazon Forest (three cities) (see Table 3). As expected, Fig. 5 Number of species cited per utilitarian redundancy category in the cities of Brazil. Legend: HR highly redundant, R redundant, NVR not very redundant 123 Author's personal copy Biodivers Conserv each of these biomes supported most of the fauna sold in the local cities investigated, corroborating the finding of Alves and Rosa (2010) that resource accessibility and availability in each region influenced the choice of traded animals (Alves and Rosa 2010). For example, some species restricted to the Amazon region, including Melanosuchus niger, Podocnemis expansa and Ramphastos tucanus, are only sold in the cities of that region, such as Belém in Pará state and Boa Vista in Roraima state (Pinto and Maduro 2003; Alves and Rosa 2007, 2010) stated that the use of the local fauna may reduce the acquisition costs of the medicinal products. However, some medicinal animals are also sold in public markets even if the species involved do not occur in the region where the markets are located. For example, products from Electrophorus electricus and Trichechus inunguis, species restricted to the North region of Brazil, are also sold in other regions. Outside their home regions, the trade of E. electricus was recorded in 15 cities (one from the Mid-west and 14 from the Northeast), while T. inunguis was sold in five cities, all in the Northeast (Alves and Rosa 2007, 2010; Ferreira et al. 2009a; Oliveira et al. 2010). The trade of marine animals in cities far from the coast also illustrates this situation. Marine and estuarine species, including Oreaster reticulatus, Echinaster echinophorus, Echinometra lacunter and Hippocampus reidi, are sold in cities such as Juazeiro do Norte (in Ceará state), Caruaru and Santa Cruz do Capibaribe (both in Pernambuco state), all of which are located in the Caatinga biome, far from the coast. The trade of medicinal animals in some cities, independent of where they occur in nature, may be associated with human migration and urbanisation. Increasing urbanisation has been observed in Brazil, which has been primarily characterised by the disordered growth of urban spaces, caused by a migration toward medium-sized and large cities. Human populations migrating from rural to urban areas took with them their body of knowledge related to the use and perception of the fauna and flora. Considerable indigenous and other traditional populations now live in Brazilian urban centres (Almada 2010), and many of these try to preserve their habits and values, including the use of plants and animals as basic ingredients in their medical practices (Alves et al. 2013). As migration still occurs between rural and urban zones (and vice versa), and also between urban centres, there is a constant exchange of information. Accordingly, in a single city there are various different social groups, each bringing with them the traditional medical practices, including the species used, from the regions where they originated, thus contributing to the spread of species used into different regions. In fact, the migration process can influence the dynamics of species used in traditional medicine through trans-cultural adaptations, where wisdom and/or practices have undergone modification (the acculturation or deculturation of uses) due to these migrations. In a specific study on this theme, Ceuterick et al. (2008) investigated the use of medicinal plants in a Columbian community in London, England. They illustrated a tendency for transcultural adaptations, reporting that the plants used by Colombians living in London were employed to treat 53 types of illnesses and/or symptoms, while the literature documents these same plants being used to treat 206 types of diseases and/or symptoms in Colombian cities. In addition to the biological and cultural aspects, the socio-economic mechanisms of commerce, such as demand, also influence the market dynamics regarding the choice and commercialisation of medicinal animals. The search for natural products by people who do not have the financial means to purchase allopathic drugs generates a demand that culminates in the trade of wild animals in several places, even when there are laws against this activity (Alves and Rosa 2010). 123 Author's personal copy Biodivers Conserv Grouping analysis (Fig. 6) showed the formation of various groups among the cities where research on the trade of zootherapeutic products was carried out. In some cases, it was observed that those cities with greater similarity were geographically close to each other, probably reflecting the influence of biological (faunal biodiversity of local biomes), cultural and social aspects (ethnic composition of the local population, socio-economic aspects, etc.). In other cases, there was a pairing of geographically distant cities, as in the grouping of Boa Vista with some cities from the Brasilia, and of Fortaleza with Salvador and Aracaju. The grouping of geographically distant cities can be explained by the existence of commercial routes of medicinal animal species between Brazilian cities (Alves and Rosa 2010), allowing medicinal animals to be sold in public markets, even if they do not occur in the regions where the markets are located. Conservation of species traded for medicinal purposes in Brazil Amongst those medicinal animals sold in Brazil, 62 species are included in categories of the Red List of endangered species (IUCN 2011). Of these species, 11 (8.3 %) are included in categories of greater concern with regards to conservation: critically endangered (CR; 2 species;1.5 %), endangered (EN;1 species; 0.7 %) and vulnerable (VU; 8 species; 6.1 %). Fig. 6 Cluster analysis of the species cited in the surveyed cities (Correlation coefficient: R = 0.84). Legend: BV Boa Vista, Be Belém, FS Feira de Santana, JP João Pessoa, CG Campina Grande, Na Natal, Te Teresina, Ca Caruaru, SCC Santa Cruz do Capibaribe, JN Juazeiro do Norte, Cra Crato, RE Recife, BR Distrito Federal, SL São Luiz, Ma Maceió, Fo Fortaleza, Ar Aracaju, Sa Salvador 123 Author's personal copy Biodivers Conserv However, 51 species are present in categories of relatively limited concern: near threatened (NT; 3 species; 2.2 %), least concern (LC; 42 species; 32 %) and data deficient (DD; 6 species; 4.5 %). Furthermore, 31 species (24.6 %) are included on the list of the International Convention of the Trade of Endangered Species (CITES 2012): Appendix I (7 species), Appendix II (22 species) and Appendix III (2 species). Despite the trade of wild animals, including species that are present on the list of endangered species, being forbidden in Brazil, it has been demonstrated that this activity remains common in some Brazilian cities, occurring illicitly and without due monitoring by competent environmental agencies. Although the medicinal trade in Brazil is not considered a threat, for most of the species sold in Brazil this activity represents an additional pressure on natural populations and, therefore, must be monitored, especially in the case of species that are particularly exploited. However, it is important to note that most zootherapeutic products are byproducts from animals hunted for other purposes (Moura and Marques 2008), such that the real motivation for capturing medicinal animals cannot be their medicinal use, as indicated by some authors (Alves et al. 2007; Ferreira et al. 2009b). The lack of monitoring of the trade of animals used for therapeutic purposes in Brazil may have serious impacts on the conservation of the species involved, as is the case in certain other countries, where the trade of animals (including for medicinal purposes) has been shown to be one of the main threats to wild populations (Lee 1999; Lee et al. 2005; Athiyaman 2008; Zhang et al. 2008; Whiting et al. 2011; Alves et al. 2013). The current scenario concerning the trade of medicinal animals in Brazil has illustrated the need for conservation strategies that support the sustainable use of these resources. Competent environmental agencies could stimulate the medicinal use and trade of domestic animal products instead of wild animal products. It is noteworthy that the breeding of domestic animals is primarily related to meat consumption and many of their by-products (which are widely used in traditional medicine) are discarded. Amongst the medicinal species sold in Brazil, 14 are domestic animals. A comparison of the RI values of domestic and wild species indicates there is no significant difference between the two groups (H = 2.2; p [ 0.05), which may favour possible substitutions. Since RI calculations assume that the most versatile species are also the most culturally important, it can probably be inferred there are no cultural differences between the use of wild and domestic species. Consequently, providing incentives to trade medicinal products (such as fat, skin and horns) from domestic species that are already raised for several other purposes (including food and clothing) could reduce possible impacts to commercialised wild species in Brazil. According to Alves et al. (2008b), a viable proposal could be the creation of cooperatives in rural communities to breed animals for medicinal markets. The cooperatives could breed any number of species for commercial purposes, with the appropriate authorisation and regulation of governmental agencies and the guidance of specialists in the area (biologists, veterinarians and animal sciences technicians). Nevertheless, conservation strategies for commercialised medicinal species must take into consideration aspects other than biological and/or ecological, such as the socio-economic implications of the trade of medicinal products from animals. Poor education (resulting in limited job opportunities) has been identified as one of the main reasons that people work in the trade of medicinal animals and plants, since this activity does not require formal education (Alves et al. 2008c). The search for natural products by people who lack the financial means to purchase allopathic drugs generates a demand that culminates in the trade of wild animals in some places, even when there are laws forbidding such activity (Alves and Rosa 2010). 123 Author's personal copy Biodivers Conserv Natural products have been the basis for the development of traditional medicines and for the discoveries of many modern drugs (Alves and Rosa 2013). Thus, considerations of negative impacts on biodiversity should not be limited to the traditional (folk) use of plants or animal products, but must also extend to their exploitation by the pharmaceutical industry (Marques 1997; Alves and Albuquerque 2013; Rose et al. 2012). As pointed out by Shaw (2009), any pharmaceutical scientist who is involved in contemporary natural product research has to get involved in or at the very least become familiar with the global issues of species conservation and/or biodiversity. Final considerations Our results have demonstrated that the trade of medicinal animals in Brazil involves a large number of confirmed species (n = 131). Estimates based on this figure suggest that the actual total is at least 200 species. The results illustrate the need for further research, which should encompass a larger number of cities, especially in regions where information on this subject is currently lacking. Before conservation strategies can be established, it is first necessary to better understand how social, cultural and biological aspects interconnect to shape or determine which species are used, the reasons behind the most frequent use of particular animal parts, and what makes a person buy an animal product for medicinal purposes. Aspects regarding public health and the pharmacological validation of zootherapeutic products must also be evaluated. Entire animals, or parts thereof, are mostly stored in unhygienic conditions, where they are exposed to light and heat (Alves and Rosa 2005). Thus, the unsanitary conditions to which marketed zootherapeutic products are exposed may facilitate the spread of diseases (zoonoses), which may be transmitted to human beings through the animal products. For example, Magnino et al. (2009) demonstrated that a considerable number of reptiles can transmit bacteria and helminths via certain parts of their bodies (such as the skin, carapace and blood). As has been presented in our review, reptiles and other vertebrates comprise a considerable proportion of the popular therapeutic armoury sold in Brazilian markets, with no monitoring of their sanitary conditions (Alves and Rosa 2007; Alves et al. 2008a). This situation is exacerbated by the fact that this trade generally occurs illicitly. Associated with the need to evaluate the sanitary conditions of marketed zootherapeutic products, it is also necessary to understand the real biological properties of the zootherapeutic products, focusing on species that are sold for medicinal purposes without any evidence of their effectiveness (Ferreira et al. 2009a). Considering the number of zootherapeutic products sold for use in traditional Brazilian medicines, there continue to be few laboratory studies into their pharmaceutical potential (Ferreira et al. 2009b, 2010, 2011). This illustrates the need for pharmacological tests to evaluate the effectiveness of animal treatments for various illnesses. Additional studies concerning zootherapeutic products must be conducted, since an understanding of the fauna sold for medicinal purposes is central to the conservation and rational use of the species involved. Certainly, research into the trade of zootherapeutic products is fundamental to the determination of appropriate practices for the handling of fauna with utilitarian purposes. In this way, traditional knowledge can help solve community problems and achieve conservationist goals. Acknowledgments The authors would like to thank the CAPES (Cordenação de Aperfeiçoamento de Pessoal de Nı́vel Superior) for the scholarships to Felipe S. Ferreira, Samuel V. Brito and Hugo Fernandes- 123 Author's personal copy Biodivers Conserv Ferreira and CNPq (ConselhoNacional de Desenvolvimento Cientı́fico e Tecnológico) for the scholarships to Nivaldo A. Léo-Neto and for providing a research fellowship to the Rômulo R. N. Alves. References Alberti M (2005) The effects of urban patterns on ecosystem function. Int Reg Sci Rev 28(2):168–192 Albuquerque UP, Oliveira RF (2007) Is the use-impact on native caatinga species in Brazil reduced by the high species richness of medicinal plants? J Ethnopharmacol 113(1):156–170 Albuquerque UP, Lucena RFP, Monteiro JM, Florentino ATN, Almeida CFCBR (2006) Evaluating two quantitative ethnobotanical techniques. Ethnobot Res Appl 4:51–60 Albuquerque UP, Monteiro JM, Ramos MA, Amorim ELC (2007a) Medicinal and magic plants from a public market in northeastern Brazil. J Ethnopharmacol 110(1):76–91 Albuquerque UP, Medeiros PM, Almeida ALS, Monteiro JM, Lins Neto EMF, Melo JG (2007b) Medicinal plants of the caatinga (semi-arid) vegetation of NE Brazil: a quantitative approach. J Ethnopharmacol 114:325–354 Almada ED (2010) Sociobiodiversidade Urbana: por uma etnoecologia das cidades. In: Silva VA, Almeida ALS, Albuquerque UP (eds) Etnobiologia e etnoecologia: pessoas & natureza na América Latina. NUPEEA, Recife, pp 39–63 Almeida CFCBR, Albuquerque UP (2002) Uso e conservação de plantas e animais medicinais no Estado de Pernambuco (Nordeste do Brasil): um estudo de caso. Interciencia 27:276–285 Alves RRN (2008) Animal-based remedies as complementary medicine in Brazil. Res Complement Med 15(4):226–227 Alves RRN (2010) O comércio de recursos zooterápicos. In: Costa Neto EM, Alves RRN (eds) Zooterapia: os animais na medicina popular brasileira. NUPEEA, Recife, pp 159–176 Alves RRN (2012) Relationships between fauna and people and the role of ethnozoology in animal conservation. Ethnobiol Conserv 1:1–69 Alves RRN, Albuquerque UP (2013) Animals as a source of drugs: bioprospecting and biodiversity conservation. In: Alves RRN, Rosa IL (eds) Animals in traditional folk medicine: implications for conservation, vol 1. Springer Heidelberg, pp 67–89 Alves RRN, Alves HN (2011) The faunal drugstore: animal-based remedies used in traditional medicines in Latin America. J Ethnobiol Ethnomed 7(1):9 Alves RRN, Rosa IL (2005) Why study the use of animal products in traditional medicines? J Ethnobiol Ethnomed 1(1):5 Alves R, Rosa IL (2007) Zootherapy goes to town: the use of animal-based remedies in urban areas of NE and N Brazil. J Ethnopharmacol 113(3):541–555 Alves RRN, Rosa IL (2010) Trade of animals used in Brazilian traditional medicine: trends and implications for conservation. Hum Ecol 38:691–704 Alves RRN, Rosa IL (2013) Animals in traditional folk medicine: implications for conservation, vol 1. Springer-Verlag, Berlin Heidelberg Alves RRN, Rosa IL, Santana GG (2007) The role of animal-derived remedies as complementary medicine in Brazil. Bioscience 57(11):949–955 Alves RRN, Lima HN, Tavares MC, Souto WMS, Barboza RRD, Vasconcellos A (2008a) Animal-based remedies as complementary medicines in Santa Cruz do Capibaribe, Brazil. BMC Complement Altern Med 8(1):44 Alves RRN, Vieira WLS, Santana GG (2008b) Reptiles used in traditional folk medicine: conservation implications. Biodivers Conserv 17(8):2037–2049 Alves RRN, Silva CC, Alves HN (2008c) Aspectos sócio-econômicos do comércio de plantas e animais medicinais em área metropolitanas do Norte e Nordeste do Brasil. Revista de Biologia e Ciências da Terra 8(1):181–189 Alves RRN, Léo-Neto NA, Brooks SE, Albuquerque UP (2009) Commercialization of animal-derived remedies as complementary medicine in the semi-arid region of northeastern Brazil. J Ethnopharmacol 124:600–608 Alves RRN, Oliveira MGG, Barboza RRD, Lopez LCS (2010) An ethnozoological survey of medicinal animals commercialized in the markets of Campina Grande, NE Brazil. Hum Ecol Rev 17(1):11–17 Alves RRN, Rosa IL, Albuquerque UP, Cunningham AB (2013) Medicine from the Wild: an overview of the use and trade of animal products in traditional medicines. In: Alves RRN, Rosa IL (eds) Animals in traditional folk medicine: implications for conservation. Springer-Verlag, Berlim, pp 25–42 123 Author's personal copy Biodivers Conserv Andrade JN, Costa-Neto EM (2006) O comércio de produtos zooterápicos na cidade de Feira de Santana, Bahia, Brasil. Sitientibus Série Ciências Biológicas (Etnobiologia) 6:37–43 Apaza L, Godoy R, Wilkie D, Byron E, Huanca T, Leonard WR, Peréz E, Reyes-Garcı́a V, Vadez V (2003) Markets and the use of wild animals for traditional medicine: a case study among the Tsimane’Amerindians of the Bolivian rain forest. J Ethnobiol 23(1):47–64 Ashwell D, Walston N (2008) An overview of the use and trade of plants and animals in traditional medicine systems in Cambodia, 1st edn. TRAFFIC Southeast Asia, Greater Mekong Programme, Ha Noi Athiyaman A (2008) An exploration into modeling sustainable consumption: the case of animal-based traditional medicines. Acad Mark Stud 2:16–23 Begossi A (1996) Use of ecological methods in ethnobotany: diversity indices. Econ Bot 50:280–289 Bennett BC, Prance GT (2000) Introduced plants in the indigenous pharmacopoeia of Northern South America. Econ Bot 54(1):90–102 Bérnils RS, HC Costa (Org.) (2012) Répteis brasileiros: Lista de espécies. Versão 2012.1. Available in http://www.sbherpetologia.org.br/. Sociedade Brasileira de Herpetologia. Accessed on 25 Oct 2012 Buckup PA, Menezes NA, Ghazzi MS (eds) (2007) Catálogo das espécies de peixes de água doce do Brasil. Museu Nacional, Rio de Janeiro Ceuterick M, Vandebroek I, Torry B, Pieroni A (2008) Cross-cultural adaptation in urban ethnobotany: the Colombian folk pharmacopoeia in London. J Ethnopharmacol 120(3):342–359 Chao A, Chazdon RL, Colwell RK, Shen TJ (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8:148–159 CITES (2012) UNEP-WCMC. UNEP-WCMC species database: CITES-listed species on the World Wide Web. Available in: http://www.unep-wcmc-apps.org/isdb/CITES/Taxonomy/index.cfm/isdb/CITES/ Taxonomy/index.cfm?displaylanguage=eng. Accessed on 25 May 2012 Colwell RK (2009) EstimateS 8.2: statistical estimation of species richness and shared species from samples. User’s Guide and Application. Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond 345:101–118 Comitê Brasileiro de Registros Ornitológicos (2011) Listas das aves do Brasil. 10a Ed. 25/1/2011, Available in http://www.cbro.org.br. Accessed on 25 Oct 2012 Costa-Neto EM (1999) Healing with animals in Feira de Santana city, Bahia, Brazil. J Ethnopharmacol 65:225–230 Costa Neto EM, Motta PC (2010) Animal species traded as ethnomedicinal resources in the Federal District, Central West Region of Brazil. Open Complement Med J 2:24–30 El-Kamali HH (2000) Folk medicinal use of some animal products in Central Sudan. J Ethnopharmacol 72(1/2):279–282 Ferreira FS, Brito SV, Ribeiro SC, Saraiva AAF, Almeida WO, Alves RRN (2009a) Animal-based folk remedies sold in public markets in Crato and Juazeiro do Norte, Ceará, Brazil. BMC Complement Altern Med 9(1):17 Ferreira FS, Brito SV, Costa JGM, Alves R, Coutinho HDM, Almeida WO (2009b) Is the body fat of the lizard Tupinambis merianae effective against bacterial infections? J Ethnopharmacol 126(2):233–237 Ferreira FS, Brito SV, Saraiva RA, Araruna MKA, Menezes IRA, Costa JGM, Coutinho HDM, Almeida WO, Alves R (2010) Topical anti-inflammatory activity of body fat from the lizard Tupinambis merianae. J Ethnopharmacol 130(3):514–520 Ferreira FS, Silva NLG, Matias EFF, Brito SV, Oliveira FG, Costa JGM, Coutinho HDM, Almeida WO, Alves RRN (2011) Potentiation of aminoglycoside antibiotic activity using the body fat from the snake Boa constrictor. Rev Bras Farmacognosia 21(3):503–509 Ferreira FS, Albuquerque UP, Coutinho HDM, Almeida WO, Alves RRN (2012) The trade in medicinal animals in northeastern Brazil. Evid Based Complement Alternat Med 2012:1–20 Freire FC (1996) Répteis utilizados na medicina popular no Estado de Alagoas. Monografia de Graduação, Universidade Federal de Alagoas Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9 IBGE (2012) The Brazilian Institute of Geography and Statistics. http://www.ibge.gov.br. Accessed on 25 Oct 2012 IUCN (2011) IUCN red list of threatened species. Version 2012 http://www.iucnredlist.org. Accessed on 05 May 2012 Jain S (2000) Human aspects of plant diversity. Econ Bot 54(4):459–470 Kang S, Phipps M (2003) A question of attitude: South Korea’s traditional medicine practitioners and wildlife conservation, 1st edn. TRAFFIC East Asia, Hong Kong 123 Author's personal copy Biodivers Conserv Lee SKH (1999) Trade in traditional medicine using endangered species: an international context. In: Proceedings of the second Australian symposium on traditional medicine and wildlife conservation, Melbourne, 1999 Lee RJ, Gorog AJ, Dwiyahreni A, Siwu S, Riley J, Alexander H, Paoli GD, Ramono W (2005) Wildlife trade and implications for law enforcement in Indonesia: a case study from North Sulawesi. Biol Conserv 123(4):477–488 Lev E, Amar Z (2000) Ethnopharmacological survey of traditional drugs sold in Israel at the end of the 20th century. J Ethnopharmacol 72(1–2):191–205 Lev E, Amar Z (2002) Ethnopharmacological survey of traditional drugs sold in the Kingdom of Jordan. J Ethnopharmacol 82(2–3):131–145 Magnino S, Colin P, Dei-Cas E, Madsen M, McLauchlin J, Nöckler K, Prieto Maradona M, Tsigarida E, Vanopdenbosch E, Van Peteghem C (2009) Biological risks associated with consumption of reptile products. Int J Food Microbiol 134(3):163–175 Mahawar MM, Jaroli DP (2008) Traditional zootherapeutic studies in India: a review. J Ethnobiol Ethnomed 4(1):1–12 Marques JGW (1997) Fauna medicinal: recurso do ambiente ou ameaça à biodiversidade? Mutum 1(1):4 Mati E, de Boer H (2011) Ethnobotany and trade of medicinal plants in the Qaysari Market, Kurdish Autonomous Region, Iraq. J Ethnopharmacol 133(2):490–510 Menezes NA, Buckup PA, Figueiredo JL, Moura RL (eds) (2003) Catálogo das espécies de peixes marinhos do Brasil. Museu de Zoologia USP, São Paulo, p 160 Monteiro JM, Araújo EL, Amorim ELC, Albuquerque UP (2010) Local markets and medicinal plant commerce: a review with emphasis on Brazil. Econ Bot 64(4):352–366 Moura FBP, Marques JGW (2008) Zooterapia popular na Chapada Diamantina: uma medicina incidental. Cienc Saude Coletiva 13(2):2179–2188 Oliveira ES, Torres DF, Brooks SE, Alves RRN (2010) The medicinal animal markets in the metropolitan region of Natal City, Northeastern Brazil. J Ethnopharmacol 130(1):54–60 Paglia AP, Fonseca GAB, Rylands AB, Herrmann G, Aguiar LMS, Chiarello AG, Leite YLR, Costa LP, Siciliano S, Kierulff MCM, Mendes SL, Tavares V C, Mittermeier RA, Patton JL (2012) Lista anotada dos mamı́feros do Brasil/Annotated Checklist of Brazilian Mammals. 2a Edição/2nd edn. Occasional Papers in Conservation Biology, No. 6. Conservation International, Arlington Pinto AAC, Maduro CB (2003) Produtos e subprodutos da medicina popular comercializados na cidade de Boa Vista, Roraima. Acta Amazonica (Brasil) 33(2):281–290 Rafael JA, Aguiar AP, Amorim DS (2009) Knowledge of insect diversity in Brazil: challenges and advances. Neotrop Entomol 38(5):565–570 Rose J, Quave CL, Islam G (2012) The four-sided triangle of ethics in bioprospecting: pharmaceutical business, international politics, socio-environmental responsibility and the importance of local stakeholders. Ethnobiol Conserv 1(3):1–25 Scarff FR, Bradley S (2002) Ecosystem function and species loss—a microcosm study. J Biogeogr 29:641–651 Shaw C (2009) Advancing drug discovery with reptile and amphibian venom peptides: venom-based medicines. Biochem Soc 31:34–37 Silva MLV, Alves ÂGC, Almeida AV (2004) A zooterapia no Recife (Pernambuco): uma articulação entre as práticas e a história. Biotemas 17:95–116 Silva VA, Nascimento VT, Medeiros MTF, Albuquerque UP, Soldati GT (2010) Técnicas para análise de dados etnobiológicos. In: Albuquerque UP, Lucena RFP, Cunha LVF (eds) Métodos e técnicas na pesquisa etnobiológica e etnoecológica. NUPEEA, Recife, pp 187–206 Sodeinde OA, Soewu DA (1999) Pilot study of the traditional medicine trade in Nigeria. Traffic Bull 18(1):35–40 Soewu DA (2008) Wild animals in ethnozoological practices among the Yorubas of southwestern Nigeria and the implications for biodiversity conservation. Afr J Agric Res 3(6):421–427 Sokal RR, Rholf FG (1995) Biometry. Freeman and Company, New York Van den Berg M (1984) Ver-o-peso: the ethnobotany of an Amazonian market. In: Kallunk P (ed) Advances in economic botany. Ethnobotany in the neotropics. New York Botanical Garden, New York, pp 140–149 Van NDN, Tap N (2008) An overview of the use of plants and animals in traditional medicine systems in Vietnam, 1st edn. TRAFFIC Southeast Asia, Greater mekong programme, Ha Noi Vázquez PE, Méndez RM, Guiascón OGR, Piñera EJN (2006) Uso medicinal de la fauna silvestre en los Altos de Chiapas, México. Interciencia 31(7):491–499 Wellnitz T, Poff NL (2001) Functional redundancy in heterogeneous environments: implications for conservation. Ecol Lett 4:177–179 123 Author's personal copy Biodivers Conserv Whiting MJ, Williams VL, Hibbitts TJ (2011) Animals traded for traditional medicine at the Faraday market in South Africa: species diversity and conservation implications. Journal of Zoolog 284:84–96 WHO (2012) World Health Organization. http://www.who.int/en/. Accessed on 10 April 2012 Williams VL, Balkwill K, Witkowski ETF (2000) Unraveling the commercial market for medicinal plants and plant parts on the Witwatersrand, South Africa. Econ Bot 54(3):310–327 Williams VL, Witkowski ETF, Balkwill K (2007) The use of incidence-based species richness estimators, species accumulation curves and similarity measures to appraise ethnobotanical inventories from South Africa. Biodivers Conserv 16(9):2495–2513 Zhang L, Hua N, Sun S (2008) Wildlife trade, consumption and conservation awareness in southwest China. Biodivers Conserv 17(6):1493–1516 123