Biodivers Conserv (2013) 22:839–870 DOI 10.1007/s10531-013-0475-7

REVIEW PAPER

The trade of medicinal in Brazil: current status and perspectives

Felipe S. Ferreira • Hugo Fernandes-Ferreira • Nivaldo A. Le´o Neto • Samuel V. Brito • Roˆmulo R. N. Alves

Received: 16 May 2012 / Accepted: 20 March 2013 / Published online: 29 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 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. Le´o Neto S. V. Brito Programa de Po´s-Graduac¸a˜o em Cieˆncias Biolo´gicas (Zoologia), Departamento de Sistema´tica e Ecologia, Centro de Cieˆncias Exatas e da Natureza, Universidade Federal da Paraı´ba (UFPB), Campus I, Joa˜o Pessoa, PB 58051-900, Brazil e-mail: [email protected]

R. R. N. Alves Departamento de Biologia, Universidade Estadual da Paraı´ba, Campina Grande, PB, Brazil 123 840 Biodivers Conserv (2013) 22:839–870 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 phar- maceutical 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;Va´zquez 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 mainte- nance 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 (Va´zquez 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 Biodivers Conserv (2013) 22:839–870 841 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 ? com- mercialization ? 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 [Ceara´ state]; Joa˜o Pessoa and Campina Grande [Paraı´ba state]; Sa˜o Luı´s [Maranha˜o state]; Teresina [Piauı´ state]; Recife, Caruaru and Santa Cruz do Capibaribe [Pernambuco state]; Maceio´ [Alagoas state]; Aracaju [Sergipe state]; Natal [Rio Grande do Norte state]; Feira de Santana and Salvador [Bahia state]); North (Bele´m [Para´ state] and Boa Vista [Roraima state]); Midwest (Planaltina, Guara´ 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 123 842 Biodivers Conserv (2013) 22:839–870

Fig. 1 Map demonstrating the locations of the studies examined in this work vertebrates] and [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 Biodivers Conserv (2013) 22:839–870 843 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 eth- nozoological 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 pro- gram (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 Albu- querque 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 indi- cates 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).

123 844 Biodivers Conserv (2013) 22:839–870

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: 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;Be´rnils 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) (Comiteˆ Brasileiro de Registros Ornitolo´gicos, 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 idvr osr 21)2:3–7 845 22:839–870 (2013) Conserv Biodivers Table 1 Animal species commercialized for medicinal purposes in Brazil Class/family/species/local name RI Part used Cities References

Cnidarians Class Hydrozoa Physaliidae Physalia physalis, Portuguese-man-of-war, 0.10 Whole animal Be 1 caravela Molluscs Class Gastropoda Achatinidade Achatina fulica, Giant east African snail, caramujo 0.10 Shell As 2 gigante africano Strombidae Strombus pugilis, West Indian fighting conch, 0.20 Shell Ar; Sa 2 estrombo-lutador- das-I´ndias-Ocidentais Class Bivalvia Cardiidae Trachycardium muricatum, Yellow prickly cockle, 0.10 Shell Sa 2 rala-coˆco Mytilidae Mytella guyanensis, Mussel, sururu 0.10 Flesh and shell SL 1 Ostreidae Crassostrea rhizophorae, Mangrove oyster, ostra 0.10 Shell Be; SL 1 do mangue Crustaceans Calappidae 123 Malacostraca Calappa ocellata, Ocellate box , 0.20 Whole animal Re 3 caranguejo-goja´ 4 idvr osr 21)22:839–870 (2013) Conserv Biodivers 846 123 Table 1 continued

Class/family/species/local name RI Part used Cities References

Squillidae Cloridopsis dubia, Mud mantis, barata-do-mar 0.10 Whole animal FS 4 Insects Class Insecta Apidae Apis mellifera, Honey bee, abelha italiana 0.98 Honey and wax Ar; Fo; Ma; Re; Sa; Cra; JN; CG; Ca; 1; 2; 5; 6; 7; 8; SCC; Te; Na; SL; Be 9 Frieseomelitta varia, Bee, abelha moc¸a branca 0.10 Honey SCC 8 Melipona compressipes, Stingless bee, tiu´ba 0.43 Honey Te; SL; Be 1 Melipona scutellaris, Stingless bee, uruc¸u´ 1.18 Honey and wax Ma; Re; Cra; JN; CG; Ca; SCC; Na; 1; 2; 5; 6; 7; 9; SL; Be 10 Melipona subnitida, Stingless bee, jandaı´ra 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 0.13 Honey Na; Be; SCC 1; 8; 9 mosquito Trigona spinipes, Stingless bee, arapua´ 0.25 Honey and wax Na; Be, FS 1; 4; 9 Blattidae Periplaneta americana, Cockroach, barata 0.30 Viscera, wings and whole Ar; Cra; JN; Ca; SCC 2; 5; 7; 8 animal Chrysomelidae Coraliomela brunnea, Fake cockroach, barata de 0.10 Whole animal CG; JP 1; 6 coqueiro Formicidae Dinoponera quadriceps, Bullet ant, trinca-cunha˜o 0.20 Whole animal CG; JN 5; 6 Gryllidae Gryllus assimilis, Cricket, grilo 0.10 Leg Cra; JN 5 Muscidae idvr osr 21)2:3–7 847 22:839–870 (2013) Conserv Biodivers Table 1 continued

Class/family/species/local name RI Part used Cities References

Musca domestica, House fly, mosca 0.10 Whole animal SCC 8 Tenebrionidae Palembus dermestoides, peanut beetle, 0.13 Whole animal Br 11 besouro-do-amendoim, Termitidae Nasutitermes corniger, Termite, cupim 0.17 Whole animal Fo 2 Nasutitermes macrocephalus, Termite, 0.13 Whole animal Ca; SCC 7; 8 cupim de aroeira Class Asteroidea Echinasteridae 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 Oreasteridae Oreaster reticulatus, Sea star, estrela do mar 0.63 Whole animal Ar; Fo; Ma; Re; Sa; JN; JP; CG; Ca; 1; 2; 6; 7; 8; 9 SCC; Na; Te; SL; Be Luidiidae Luidia senegalensis, Sea star, estrela-do-mar 0.20 Whole animal JP; CG; Ca 1; 6; 7; 10 Class Echinoidea Echinometridae Echinometra lucunter, Rock boring urchin, 0.10 Whole animal Ca; Re 3; 7 ouric¸o-do-mar Mellitidae

123 Mellita quinquiesperforata, , 0.10 Whole animal Ca 7 bolacha-de-praia Class 4 idvr osr 21)22:839–870 (2013) Conserv Biodivers 848 123 Table 1 continued

Class/family/species/local name RI Part used Cities References

Anostomidae Leporinus steindachneri, Black piau, piau 0.10 Fat Cra; JN 5 Balistidae Balistes vetula, Queen triggerfish, cangulo, VU* 0.20 Skin SL 1 Erythrinidae Hoplias malabaricus, Trahira, traı´ra 1.06 Fat Ar; Fo; Cra; CG; SCC; Te; FS; Na 1; 2; 4; 6; 8; 9 Gymnotidae Electrophorus electricus, Electric , 1.37 Fat Ar; Fo; Ma; Re; Sa; JN; Ca; SCC; 1; 2; 4; 5; 7; 8; peixe ele´trico, LC SL; Te; FS; Na; Be; BV; Br 9; 11; 12 Megalopidae Megalops atlanticus, Tarpon, camurupim 0.10 Scale SL; Be 1 Osteoglossidae Arapaima gigas, Giant arapaima, pirarucu, 0.10 Scale Be 1 DD*, II Pimelodidae Phractocephalus hemioliopterus, Redtail Catfish, 0.13 Fat BV 12 pirarara Sciaenidae Cynoscion acoupa, Acoupa weakfish, 0.13 Otolith SL 1 pescada amarela, LC Cynoscion leiarchus, Smooth weakfish, 0.13 Otolith SL 1 pescada branca Syngnathidae Hippocampus reidi, Longsnout seahorse, 1.05 Whole animal Ar; Fo; Ma; Re; Sa; JN; JP; CG; Ca; 1; 2; 4; 6; 7 cavalo marinho DD, II SCC; SL; Te; FS; Na; Be Prochilodontidae idvr osr 21)2:3–7 849 22:839–870 (2013) Conserv Biodivers Table 1 continued

Class/family/species/local name RI Part used Cities References

Prochilodus nigricans, Black prochilodus, 0.10 Fat Cra; JN 5 curimata˜ Tetraodontidae Sphoeroides testudineus, Checkered puffer, baiacu 0.10 Fat FS 4 Class Elasmobranchii Carcharhinidae Carcharhinus limbatus, Blackfin shark, 0.10 Cartilage SL 1 sucuri preto NT Carcharhinus leucas, Cub shark, tubara˜o, NT – – Ca 10 Pristidae Pristis pectinata, Sawfish, Smalltooth sawfish, 0.23 Rostral expansion Be 1 espadarte CR, I Pristis perotteti, Largetooth sawfish, espadarte, 0.23 Rostral expansion Be 1 CR, I Amphibians Class Amphibia Bufonidae Rhinella jimi Cururu toad, sapo cururu, LC 0.98 Secretions, fat and skin Ar; Fo; Re; Sa; SCC 2; 8 Leptodactylidae Leptodactylus labyrinthicus, South American 0.15 Fat Fo 2 pepper frog, ra˜-pimenta, LC Leptodactylus vastus, Northeastern pepper frog, 0.28 Fat Fo 2 ra˜-pimenta, LC Reptiles 123 Class Reptilia Cheloniidae 5 idvr osr 21)22:839–870 (2013) Conserv Biodivers 850 123 Table 1 continued

Class/family/species/local name RI Part used Cities References

Chelonia mydas, Green sea turtle, tartaruga verde, 1.01 Fat and carapace Fo; Sa 2 EN, II Chelidae Phrynops geoffroanus, Geoffroy’s side-necked 0.93 Carapace and fat JP; CG; Ca; SCC; SL; Na 1; 6; 7; 8; 9 turtle, ca´gado Phrynops tuberosus, Cotinga river toadhead turtle, 0.30 Carapace and fat Cra; JN 5 ca´gado Mesoclemmys tuberculatus, Tuberculate toadhead 0.10 Carapace Ma 13 turtle, ca´gado d’a´gua Testudinidae Chelonoidis denticulata, Yellow-footed tortoise, 0.58 Carapace, fat, liver, urine and Ca; SCC; Be 1; 7; 8 jabuti VU*, II whole animal Chelonoidis carbonaria, Red-footed tortoise, 0.71 Carapace, fat, liver and blood Ca; SL; FS; Be 1; 4; 7 jabuti do pe´ vermelho, II Podocnemididae Podocnemis expansa, Amazon river turtle, 0.58 Fat Be; BV 1; 12 tartaruga da amazoˆnia LR*, II Alligatoridae Caiman crocodilus, Common caiman, jacare´-tinga 0.86 Skin, fat and tooth Cra; JP; CG; Ca; SL; Te; Be; BV 1; 5; 6; 7; 12 LR*, II Caiman latirostris, Broad-snouted caiman, jacare´ 0.96 Skin, fresh, fat, leather and JP; CG; Ca; SCC; SL; Te; Ma; FS; 1; 4; 6; 8; 9; do papo-amarelo LR*, II tooth Na 10; 13 Paleosuchus palpebrosus, Dwarf caiman, jacare´ 0.48 Skin, fresh, fat and penis JP; CG; SL; Te; Be 1; 6 coroa LR*, II Melanosuchus niger, Black caiman, jacare ac¸u´, II 0.58 Fat, skin and penis Be 1 Boidae Boa constrictor constrictor, Common boa, 1.53 Fat, bone, feces and skin Ar; Fo; Ma; Sa; JP; CG; SL; Be; BV; 1; 2; 6; 11; 12; jibo´ia, II Br 14 idvr osr 21)2:3–7 851 22:839–870 (2013) Conserv Biodivers Table 1 continued

Class/family/species/local name RI Part used Cities References

Corallus caninus, Emerald tree boa, cobra 0.10 Whole animal SL 1 papagaio, II 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, 0.66 Fat Ca; SL Te; Be; BV 1; 7; 12 sucuri, II Colubridae Oxyrhopus trigeminus, Brazilian false coral snake, 0.20 Whole animal, fat and skin CG; Ma 1; 6; 13 falsa coral Leptophis ahetula, Parrot snake, cobra cipo´ 0.10 Whole animal SL 1 Mastigodryas bifossatus, Rio tropical racer, 0.10 Whole animal Ma 13 jaracuc¸u Philhodryas olfersii, Lichtenstein’s green racer, 0.10 Whole animal Sa 2 cobra verde Spilotes pullatus, yellow snake, caninana 0.33 Bone, fat and whole animal Sa; Be 1; 2 Viperidae Crotalus durissus, rattlesnake, cascavel LC, II 1.80 Fat, rattle, bone and skin Ar; Fo; Ma; Re; Sa; Cra; JN; JP; CG; 1; 2; 3; 4; 5; 6; Re; Ca; SCC; SL; Te; Ma; FS; Na; 7; 8; 9; 11; Be; BV; Br 12; 13; 14 Lachesis muta, Bushmaster, surucucu pico de jaca 0.23 Fat Ma; Be 1; 13 Elapidae Micrurus ibiboboca, Caatinga coral snake, coral 0.50 Fat and skin Ma 2; 13 verdadeira Iguanidae Iguana iguana, Common green iguana camalea˜o, 0.75 Fat, bone and tail Ma; Re; CG; Ca; SCC; SL; Na; Be 1; 2; 6; 8; 9;

123 II 10 Gekkonidae Hemidactylus mabouia, House gecko, lagartixa 0.10 Whole animal CG 1 Teiidae 5 idvr osr 21)22:839–870 (2013) Conserv Biodivers 852 123 Table 1 continued

Class/family/species/local name RI Part used Cities References

Ameiva ameiva, Giant ameiva, calango bico doce 0.10 Whole animal Ma 13 Cnemidophorus ocelifer, Spix’s whiptail calango 0.35 Whole animal Ma 1; 13 Tupinambis merianae, Teju lizard, tiu´ LC, II 1.62 Fat, skin and tail Ar; Fo; Ma; Re; Sa; Cra; JN; JP; CG; 1; 2; 5; 6; 7; 8; Ca; SCC; Te; Na 9 Tupinambis teguixin, Teju lizard, tejuac¸u´, II 0.91 Fat, tail, skin, eggs, meat and SL; Be; Ma 1; 13 bone Tropiduridae Tropidurus hispidus, Lizard, lagartixa 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 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 Cathartidae Coragyps atratus, Black vulture, urubu, LC 0.45 Feather, liver, beak and fat Fo; Ma; Re; JN; JP; Ca; SCC; SL; 1; 2; 6; 7; 8 Te; Be Cyanocorax cyanopogon, White-naped jay, 0.10 Whole animal SCC 8 canca˜o, LC Columbidae Columba livia, Rock pigeon, pombo, LC 0.17 Fat Sa 2 Cuculidae Crotophaga ani, Smooth-billed ani, anu, LC 0.10 Whole animal and fresh Cra; SL 1; 5 Pipridae Pipra aureola, Crimson-hooded manakin, 0.10 Fat BV 12 uirapuru, LC Phasianidae idvr osr 21)2:3–7 853 22:839–870 (2013) Conserv Biodivers Table 1 continued

Class/family/species/local name RI Part used Cities References

Gallus gallus, Chicken, galinha, LC 1.46 Fat, spur and gizzard Ar; Fo; Re; Sa; Cra; JN; JP; CG; Ca; 1; 2; 4; 5; 6; 7; SCC; SL; Te; FS; Na; Be; BV; Br 8; 9; 10; 11; 12 Pavo cristatus, Common peafowl, pava˜o, LC 0.53 Feather and fat Sa; Cra; Ca; SCC; FS; Ma 2; 5; 8; 10; 14 Numida meleagris, Helmeted guineafowl, Guine´, 0.40 Fat and blood Sa; Ca; SCC; Br 2; 6; 8; 11 LC Meleagris gallopavo, Wild turkey, peru, LC 0.87 Feather Ca 8 Ramphastidae Ramphastos tucanus, White-throated toucan, 0.10 Beak Be 1 tucano, LC, II Rheidae Rhea americana, Greater rhea, ema, NT, II 0.58 Fat and skin Re; JP; CG; Ca; FS; Na; Be; Br 1; 2; 6; 7; 10; 14 Struthionidae Struthio camelus, Common ostrich, avestruz, LC 0.10 Eggs shells SCC 8 Tinamidae Nothura maculosa cearensis, Spotted nothura, 0.10 Feather SCC 8 codorniz Mammals Class Mammalia Agoutidae Cuniculus paca, Spotted paca, paca, LC, III 0.58 Fat, penis and bile Sa; SL; Be; BV; Br 1; 2; 12; 13 Bovidae Bos taurus, Cow, boi 1.13 Fat, tail, skin, urine, penis, Fo; Ma; Re; Sa; C; JN; Ca; SCC; SL; 1; 2; 3; 5; 10; 123 horn and bile Te; FS; Br; BV 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; 1; 2; 3; 5; 6; 7; SCC; SL; Na; Be; BV; Br 8; 9; 10; 12 5 idvr osr 21)22:839–870 (2013) Conserv Biodivers 854 123 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 Bradypodidae Bradypus variegatus, Brown-throated three-toed 0.20 Skin, claw and bones Ca; Be, CG 1; 6; 7; 10 sloth, preguic¸a LC, II Canidae 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 Caviidae Kerodon rupestris, Rock cavy, moco´, LC 0.13 Fat and manure SCC 8 Cervidae Mazama gouazoubira, Gray brocket, veado 0.38 Tail, horn, nail and tibia FS; Fo; Ma; Re; Sa 2; 4 catingueiro, LC Mazama americana, Red brocket, veado gaeado, 0.10 Tibia CG; Ca 6; 10 DD Cebidae Cebus apella, Brow capuchin, macaco-prego, 0.35 Penis, bone and fat Be 1 LC, II Dasyponidae Dasypus novemcinctus, Nine-banded armadillo, 1.06 Fat, tail, leg and skin Ma; Re; Cr; JN; Ca; SL 1; 2; 5; 7 tatu galinha, LC Euphractus sexcinctus, Six-banded armadillo, 1.33 Legs, tail, urine, skin and fat Ma; Re; Sa; Cr; JN; JP; Ca; SCC; 1; 2; 5; 7; 8; 9 tatu peba, LC SL; Na Didelphidae Didelphis marsupialis, Common opossum, 0.25 Fat SL; Be 1 mucura, LC Didelphis albiventris, White-eared opossum, 0.20 Bone Ca; Na, CG 6; 7; 9 timbu, LC idvr osr 21)2:3–7 855 22:839–870 (2013) Conserv Biodivers Table 1 continued

Class/family/species/local name RI Part used Cities References

Equidae Equus asinus, Asino, jumento 0.33 Milk and hoof Ca; SCC; SL 1; 7; 8 Erethizontidae Coendou prehensilis, Brazilian porcupine, porco 0.93 Spines Ar; Ma; Re; Sa; JP; CG; Re; Ca; 1; 2; 3; 4; 6; 7; espinho, LC SCC; SL; Te; FS; Be 8 Coendou bicolor, bicolored-spined porcupine, – – Ca 10 porco espinho, LC Felidae Leopardus pardalis, Ocelot, gato maracaja´, LC, II 0.30 Eyes Re; Ca 2; 10 Hydrochoeridae Hydrochoerus hydrochaeris, Capybara, capivara, 0.63 Bone, fat and fresh SL; Te; BV; Br 1; 11; 12 LC Mustelidae Conepatus semistriatus, Striped hog-nosed skunk 0.35 Bone, fat and meat Ca; SCC 7; 8 gambamba´,LC Mymercophagidae Myrmecophaga tridactyla, Giant anteater. 0.10 Skin Sa 2 tamandua´ bandeira, VU, II Procyonidae Procyon cancrivorus, Crab-eating raccoon, 0.61 Fat and skin JN; SL; Te 1; 5 guaxinim LC Nasua nasua, South American coati, quati, LC, III 0.33 Fat and penis FS; Be 1; 4; 14 Suidae Sus scrofa, pig, porco, LC 0.23 Navel and fat Cra; Re 2; 5 123 Tapiridae Tapirus terrestris, South American tapir, anta, 0.40 Fat and paw Be; BV 1; 12 VU, II 5 idvr osr 21)22:839–870 (2013) Conserv Biodivers 856 123 Table 1 continued

Class/family/species/local name RI Part used Cities References

Tayassuidae Pecari tajacu, Collared peccary, caititu, LC, II 0.13 Fat SL 1 Phyllostomidae Desmodus rotundus, Vampire bat, morcego, LC 0.30 Whole animal Sa 2 Delphinidae Sotalia fluviatilis, Gray dolphin, boto DD, I 0.73 Fat and penis SL; Be; BV 1; 12 Sotalia guianensis, Guianan river dolphin, 1.73 Fat, penis, eyes and blood Ar; Fo; Ma; Re; Sa; SL; Be 1; 2 boto DD, I Iniidae Inia geoffrensis, Amazon river dolphin, boto rosa 0.48 Fat Be 1 DD, II Trichechidae Trichechus inunguis, Amazon manatee, peixe-boi 0.75 Fat and skin JP; Ca; SL; FS; Be 1; 4; 7 VU, I Trichechus manatus, Manatee, peixe-boi VU, I 1.80 Fat and skin Ar; Ma; Re; Sa; JP; SL; Te; Be; FS 1; 2; 4 Balaenopteridae Balaenoptera acutorostrata, Common minke 0.10 Fat JP; SL; Be 1 whale, baleia minke, LC, I Physeteridae Physeter macrocephalus, Sperm whale, cachalote, 0.10 Fat JP; SL; Be 1 VU 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 Cities: BV Boa Vista, Be Bele´m, FS Feira de Santana, JP Joa˜o 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 Sa˜o Luiz, Ma Maceio´, 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 (2013) 22:839–870 857

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) 123 858 Biodivers Conserv (2013) 22:839–870

Table 2 Estimators of species richness showing the number of species that may be marketed in Brazil Sobs ICE Chao 2 Jack 1 Jack 2

All animals 131 193 172 178 200 Wild vertebrate 87 132 120 120 137 Domestic vertebrate 14 17 15 17 18 Marine 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 Biodivers Conserv (2013) 22:839–870 859

Table 3 Overview of trade in medicinal animals in Brazil Cities Number Species most cited Biome in which References of the city is species located

Crato 22 Phrynops tuberosus Caatinga Ferreira et al. (2009a) Juazeiro do 22 Tupinambis merianae Caatinga Ferreira et al. (2009a) Norte Fortaleza 24 Apis mellifera Caatinga Ferreira et al. (2012) Joa˜o Pessoa 19 Hippocampus reidi; Atlantic forest Alves and Rosa Paleosuchus palpebrosus; (2007, 2010) Caiman crocodilus Campina 32 Gallus gallus Caatinga Alves et al. (2010) Grande Recife 27 Ovis aries Atlantic forest Silva et al. (2004) and Ferreira et al. (2012) Caruaru 34 Oreaster reticulatus; Caatinga Almeida and Albuquerque Hippocampus reidi; Caiman (2002) and Alves et al. crocodilus (2009) Sa˜o Luiz 47 Boa constrictor Amazon Forest Alves and Rosa (2007, 2010) Teresina 22 Crotalus durissus Caatinga Alves and Rosa (2007, 2010) Santa Cruz do 35 Crotalus durissus; Gallus Caatinga Alves et al. (2008a) Capibaribe gallus Aracaju 18 Echinaster echinophorus Atlantic Forest Ferreira et al. (2012) Maceio´ 25 Sotalia guianensis Atlantic Forest Freire (1996) and Ferreira et al. (2012) Natal 19 Tupinambis merianae; Atlantic Forest Oliveira et al. (2010) Cerdocyon thous Salvador 31 Hipocampos reidi Atlantic Forest Ferreira et al. (2012) Feira de 16 – Caatinga Costa-Neto (1999) and Santana Andrade and Costa-Neto (2006) Bele´m45Hippocampus reidi Amazon Forest Alves and Rosa (2007, 2010) Boa Vista 15 – Amazon Forest Pinto and Maduro (2003) Planaltina, 11 Crotalus durissus Cerrado Costa Neto and Motta Guara´ and (2010) Sobradinho 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 123 860 Biodivers Conserv (2013) 22:839–870

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;Va´zquez 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 Biodivers Conserv (2013) 22:839–870 861

Table 4 Categories of diseases Categories Number of treated with animal-based medi- medicinal cines that are sold in public animals markets in Brazil Diseases of the respiratory system 72 Undefined illnesses 53 Diseases of the musculoskeletal system 48 and connective tissue 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 11 other external causes 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 Hippo- campus reidi (longsnout seahorse), Electrophorus electricus () 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 pref- erences 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.

123 862 Biodivers Conserv (2013) 22:839–870

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 utili- tarian redundancy (Albuquerque and Oliveira 2007), the pressure exerted on animal spe- cies 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. Conse- quently, 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 Biodivers Conserv (2013) 22:839–870 863 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 avail- ability 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 Bele´m in Para´ 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 Ceara´ 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 indige- nous 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 under- gone 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 trans- cultural 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 cul- minates in the trade of wild animals in several places, even when there are laws against this activity (Alves and Rosa 2010).

123 864 Biodivers Conserv (2013) 22:839–870

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 exis- tence 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 Bele´m, FS Feira de Santana, JP Joa˜o 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 Sa˜o Luiz, Ma Maceio´, Fo Fortaleza, Ar Aracaju, Sa Salvador 123 Biodivers Conserv (2013) 22:839–870 865

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 Inter- national 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 environ- mental 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 by- products 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 calcula- tions 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 cooper- atives in rural communities to breed animals for medicinal markets. The cooperatives could breed any number of species for commercial purposes, with the appropriate au- thorisation 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). 123 866 Biodivers Conserv (2013) 22:839–870

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 zoother- apeutic products, focusing on species that are sold for medicinal purposes without any evidence of their effectiveness (Ferreira et al. 2009a). Considering the number of zoo- therapeutic 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 com- munity problems and achieve conservationist goals.

Acknowledgments The authors would like to thank the CAPES (Cordenac¸a˜o de Aperfeic¸oamento de Pessoal de Nı´vel Superior) for the scholarships to Felipe S. Ferreira, Samuel V. Brito and Hugo Fernandes- 123 Biodivers Conserv (2013) 22:839–870 867

Ferreira and CNPq (ConselhoNacional de Desenvolvimento Cientı´fico e Tecnolo´gico) for the scholarships to Nivaldo A. Le´o-Neto and for providing a research fellowship to the Roˆmulo R. N. Alves.

References

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