A review on human attitudes towards reptiles in Brazil

A review on human attitudes towards reptiles in Brazil

Rômulo Romeu Nóbrega Alves & Kleber Silva Vieira &

Gindomar Gomes Santana & Washington Luiz Silva Vieira &

Waltécio Oliveira Almeida & Wedson Medeiros Silva Souto &

Paulo Fernando Guedes Pereira Montenegro & Juarez Carlos Brito Pezzuti

Received: 15 May 2011 /Accepted: 15 November 2011 /Published online: 2 December 2011# Springer Science+Business Media B.V. 2011

Abstract For many millennia humans and reptileshave interacted, but the attitude of humans towardsthese animals has depended on culture, environment,and personal experience. At least 719 reptile speciesare known to occur in Brazil and about 11% of thisfauna has been exploited for many different purposes,including bushmeat, leather, ornamental and magic/religious uses, and as folk medicines. Brazil cantherefore serve as an interesting case study for betterunderstanding reptile use by human societies, and thepresent paper catalogues some of the reptile speciesbeing used in Brazil and discusses implications for

their conservation. A literature review indicated that81 reptile species are culturally important in thiscountry, with 47 (58%) species having multiple uses,54 being used for medicinal purposes, 38 as food, 28for ornamental or decorative purposes, 20 used inmagic/religious practices, 18 as pets, and 40 arecommonly killed when they come into contact withhumans. Regarding their conservation status, 30(37.5%) are included on State's Red List, BrazilianRed List or the IUCNRed List. There are many forms ofinteraction between reptiles and humans in Brazil—although most of them are quite negative in terms of

Environ Monit Assess (2012) 184:6877–6901DOI 10.1007/s10661-011-2465-0

R. R. N. Alves (*)Departamento de Biologia,Universidade Estadual da Paraíba,Av. das Baraúnas, 351/Campus Universitário Bodocongó,58109-753 Campina Grande, PB, Brazile-mail: [email protected]

K. S. Vieira :W. L. S. Vieira :W. M. S. SoutoDepartamento de Sistemática e Ecologiada Universidade Federal da Paraíba, Programa dePós-Graduação em Ciências Biológicas (Zoologia),Laboratório de Ecofisiologia Animal,58051-900 João Pessoa, PB, Brazil

G. G. SantanaDepartamento de Botânica, Ecologia e Zoologia,Bolsista de Desenvolvimento Científico Regional(DCR/CNPq/FAPERN), Ecologia e Zoologia,Laboratório de Ecologia e Conservação da Biodiversidade(LECOB), Centro de Biociências,Universidade Federal do Rio Grande do Norte,Lagoa Nova,59072-970 Natal, RN, Brazil

W. O. AlmeidaDepartamento de Química Biológica BolsistaProdutividade da Fundação Cearense de Apoio aoDesenvolvimento Científico e Tecnológico—FUNCAP,Universidade Regional do Cariri,Rua Cel. Antônio Luiz 1161, CEP,63100-000 Crato, CE, Brazil

P. F. G. P. MontenegroDepartamento de Sistemática e Ecologia da UniversidadeFederal da Paraíba, Laboratório de Ecofisiologia Animal,58051-900 João Pessoa, PB, Brazil

J. C. B. PezzutiNúcleo de Altos Estudos Amazônicos—NAEA,Universidade Federal do Pará—UFPA,Belem, Brazil

wildlife conservation—which reinforces the importanceof understanding such uses and interactions in thecontext of protecting reptiles in Brazil. A betterunderstanding of the cultural, social, and traditionalroles of these reptiles is fundamental to establishingmanagement plans for their sustainable use.

Keywords Conservation . Ethnozoology .

Ethnoherpetology .Wildlife use

Introduction

Evidence from a variety of sources has shown thathumans have long exploited the eggs, meat, blood,oil, shells, skins, bones, and other parts of reptiles toprovide food and materials for making tools,ornaments, medicines, and religious objects (Fitter1986; Franke and Telecky 2001; Fitzgerald et al.2004; Zhou and Jiang 2004; Frazier 2005; Alves2006a; Alves et al. 2007, 2008; Alves and PereiraFilho 2007; Alves and Santana 2008). Nonetheless,these animals are considered pests in many localities,motivating their extermination as malignant entities oras threats to humans and domestic animals (Alves etal. 2009a, b; Fita et al. 2010).

Human perceptions of reptiles are often characterizedby extremes, and different cultures may consider themeither fascinating (such as the crocodile, Sebek) orfearful (the great serpent of the land of the dead,Apófis). African (rock) pythons (Python sebae) androyal pythons (P. regius) are tabooed and worshippedin some African societies (Cansdale and Wood 1961).Snakes throughout Ghana (usually the royal python,African python, or black cobra [Naja melanoleuca])have positive taboos or totemic symbols (Attuquayefio2004). The god of the Nile River was a god-serpent,symbolizing the power of the Pharaoh (Moreno et al.2006). The caduceus (the medical symbol of twosnakes wrapped around a staff) from ancient Greekmythology originated from the mythical figure Æscu-lapius who discovered medicine as he watched onesnake healing another with herbs (Jackson and Mirick1996). In western cultures, the serpent is wrapped inmyths, legends and beliefs—perhaps the best knownof these tales being the loss of paradise by Adam andEve due to the guile of a snake (Leeming 2003).

The symbolic significance of reptiles varies greatlyamong different cultures and depends on the types of

relationships that humans have had with these animals(Campbell et al. 1991; Leeming 2003; Alves andPereira Filho 2007; Alves et al. 2008, 2009a; Vitt andCaldwell 2009; Ceríaco 2010; Ceríaco et al. 2011;Pough et al. 2004). Mystical elements can generateeither positive or negative perspectives for conser-vation, especially if these animals are feared orhated because of their association with evil;which is often the case with snakes (see DoddJr 1993; Vizotto 2003; Alves et al. 2010a; Ceríaco2010). In many cultures, these opposing visionsoverlap and result is both appreciation for, and hatredof, these animals (Alves et al. 2010a).

There are currently 721 species of reptiles knownin Brazil, of which 679 belong to the Squamata (67amphisbaenids, 371 serpents, and 241 lizards); thereare also six species of caimans and 36 species ofchelonians (Bérnils 2010). In close proportion to thisconsiderable reptilian biodiversity are the manyrelationships that exist between humans and reptiles.A significant part of this fauna was used by traditionalhuman populations, and some are still used bymodern societies. Many stories, myths, proverbs,and stories have been generated from these relation-ships and passed down from generation to generationthrough oral traditions, influencing how local peoplerelate to these animals. In Brazil, people and reptileshave interacted for millennia, coexisting in manydifferent ways, mainly because of their utility orbecause of the risks they represent. Products derivedfrom reptiles (including leather, teeth, fat, meat, andbones) have nutritional, ornamental, and medicinalvalues in many rural and urban areas in Brazil andthese animals are often sought after as pets andzoological attractions.

Ethnoherpetology, a subdivision of Ethnozoology,examines the relationships between human culturesand reptiles (Speck 1946; Goodman and Hobbs 1994;Bertrand 1997; Das 1998). Very few ethnoherpeto-logical studies have been undertaken in Brazil (Alves2006a; Alves et al. 2007a, 2009a; Alves and PereiraFilho 2007; Alves and Santana 2008; Fita et al. 2010).An important step in guaranteeing the sustainable useof the herpetofauna is understanding the relationshipsthat have been established between humans and theseanimals, including the species most frequently takenand their different uses. Ethnozoological studies arefundamental to this process and are essential toformulating conservation and management strategies,

6878 Environ Monit Assess (2012) 184:6877–6901

since reptiles are of very high importance to humanpopulations from ecological, economic, and culturalpoint of views.

The present paper presents an analysis of therelationships between Brazilian populations andsome native reptiles, focusing on the utilitarianvalue that these human groups assign to theseanimals and on conflicting relationships associatedwith this zoological group.

Procedures

Information was gathered from published articles, booksand book chapters, theses and dissertations, and under-graduate theses, as well as from reports available atinternational online databases such as Science Direct(www.sciencedirect.com), Scirus (www.scirus.com),Google Scholar, Scopus (www.scopus.com), Web ofScience (www.isiknowledge.com), and BiologicalAbstracts (science.thomsonreuters.com) using thefollowing search terms: ― reptiles+uses+Brazil ―reptiles+medicinal+Brazil― Reptiles+pets+Brazil―Reptiles+magic religious+Brazil ― reptiles+conflicts+Brazil and ethnoherpetology+reptiles+Brazil, ethnozoology+reptiles+Brazil. Scientificnames provided in publications were updatedaccording to the ITIS Catalogue of Life: 2011Annual Checklist.

Results and discussion

The use of reptiles by human populations in Brazil

Large numbers of human communities with uniquetraditions can be found within the vast territory ofBrazil. The importance and utility that these commu-nities attribute to local reptiles species is proportionalto the cultural diversity of a given region (Alves et al.2010a). The same species of lizard, for example, canbe used in different ways and for different ends bydifferent societies. Many species of Brazilian reptilesare used as foods, in popular medicines, for orna-mentation and religious purposes, and to make articlesof clothing or handicrafts; reptiles are also raised incaptivity as pets (even though this practice issomewhat less common than with birds or mammals).In general, human communities have links with at

least 81 species of reptiles throughout the country(Table 1).

Reptiles as food sources

Throughout history human populations in all parts ofthe world have consumed reptiles as importantcomponents of their diets. Reptiles are an importantsource of protein for human populations in manyparts of the world (other than Europe and NorthAmerica, where consumption is comparatively muchlower). In Europe, there is limited traditional con-sumption of reptile meat, although the ocellated lizard(Timon lepidus) was eaten in some parts of Spain upuntil just a few decades ago, and turtle soup has beena delicacy in the UK and in other European countriessince the nineteenth and early twentieth centuries(Magnino et al. 2009). Although some reptiles areeaten in temperate regions, their consumption is muchmore intense in tropical and subtropical regions(Klemens and Thorbjarnarson 1995). This differenceis probably related to the low species diversity ofreptiles in temperate zones and their low caloric value—in contrast to hyper-caloric game animals such asbovines, swine and birds (Torres et al. 2000).

At least 38 reptile species are consumed as foodin Brazil and, as can be seen in other countries(see Klemens and Thorbjarnarson 1995), there isconsiderable variation in the preferences of thesehuman populations for chelonians, caimans, lizards,and snakes.

Chelonians

Among the wide variety of wild reptiles used for foodby humans, chelonians (meat and eggs) are probablythe most heavily exploited worldwide. CharlesDarwin reported meeting a party of Spanish sailorsin 1835 on the Galapagos Archipelago who weresalting meat from giant tortoises; and whenexploring inland he and his party “lived entirelyupon tortoise meat: the breast plate roasted… withflesh on it is very good; and young tortoises makeexcellent soup” (Darwin 1854).

Subsistence use of chelonians has a long history inmany regions. Of the 36 species of chelonians inBrazil, 20 (55.5%) are eaten by humans. Theseanimals are commonly sought after as food in thenorthern region of the country where their species

Environ Monit Assess (2012) 184:6877–6901 6879

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Table 1 Reptile species, their respective uses, conflicting characteristics in Brazil, and status of conservation

Family/species/vernacular name Uses and conflictingrelationships

IUCN Brazil Red List States' Red Lists

F M MR P O CR MG RJ SP RS ES

CAYMANS

Alligatoridae

Caiman crocodilus (Linnaeus, 1758)—"jacaré tinga",Common Caiman

■ ■ ■ ■ ■ ■ LC

Caiman latirostris (Daudin, 1802) – Broad-snouted Caiman ■ ■ ■ ■ ■ ■ LC VU EN VU –a –a

Caiman yacare (Daudin, 1802)—Panama caiman,yacare caiman

■ ■ ■ ■ ■ ■ LC

Melanosuchus niger (Spix, 1825)—Black Caiman ■ ■ ■ ■ ■ CD

Paleosuchus palpebrosus (Cuvier, 1807)—“jacaré coroa”,“jacaré”, “jacaré-preto”, “crocodilo”, Cuvier'sSmooth-frontedCaiman, Dwarf Caiman

■ ■ ■ ■ ■ ■ LC EN VU

Paleosuchus trigonatus (Schneider, 1801)—“jacaré”,Schneider's Smooth-Fronted Caiman

■ ■ LC

SNAKES

Boidae

Boa constrictor Linnaeus, 1758 -“boa”,“jibóia” ■ ■ ■ ■ ■ ■ –a –a –a

Corallus caninus (Linnaeus, 1758)—“cobra papagaio” ■ ■

Corallus hortulanus (Linnaeus, 1758)—“cobra de veado”,“cobra veadeira”, Amazon Tree Boa, Common Tree Boa

■ ■ VU –a VU –a

Eunectes murinus (Linnaeus, 1758)—“sucurujú”,“sucuri”, Anaconda

■ ■ ■ ■ ■ –a –a –a –a

Eunectes notaeus Cope, 1862—Anaconda ■ ■ ■ ■ ■Epicrates assisi Machado, 1945 ■ ■ ■

Epicrates cenchria (Linnaeus, 1758)—“salamanta”,Rainbow Boa

■ ■ ■ –a –a VU –a

Colubridae

Leptophis ahaetulla (Linnaeus, 1758)—“cobra cipó” ■ –a –a –a –a

Mastigodryas bifossatus (Raddi, 1820)—“jaracuçú” ■ ■Oxybelis aeneus (Wagler, 1824)—“cobra cipó”,Brown Vine Snake

■ –a –a –a –a –a

Spilotes pullatus (Linnaeus, 1758)—“caninana”,Culebra-ratonera mica

■ ■ ■ –a –a –a –a –a

Tantilla melanocephala (Linnaeus, 1758)—“cobra rainha”,“cobra do folhiço”, Black-headed Snake

■ –a –a –a –a –a

Dipsadidae

Boiruna sertaneja Zaher, 1996—“cobra preta” ■Drymarchon corais (Boié, 1827)—Indigo Snake ■ LC

Hydrodynastes gigas (Duméril, Bibron & Duméril, 1854) ■ –a –a –a VU

Liophis viridis Günther, 1862—“cobra verde”, “cobra d’água” ■ LC

Oxyrhopus guibei Hoge & Romano, 1978 ■ ■ ■ –a –a –a –a –a

Oxyrhopus petola (Linnaeus, 1758)—Calico Snake ■ ■ ■ –a –a –a –a –a

Oxyrhopus trigeminus Duméril, Bibron & Duméril,1854—“falsa coral”, “tricolor”

■ ■ ■ –a –a

Philodryas nattereri Steindachner, 1870—“corre-campo” ■ –a –a

Philodryas olfersii (Lichtenstein, 1823)—“cobra verde”,Green snake

■ –a –a –a –a –a

Pseudoboa nigra (Duméril, Bibron & Duméril, 1854)—“cobra preta”

■ –a –a –a

Sibynomorphus neuwiedi (Ihering, 1911) ■ –a –a

Xenodon merremii (Wagler, 1824)—“focinho-de-cachorro” ■ –a –a –a –a

Elapidae

Micrurus ibiboboca (Merrem, 1820)—“cobra-coral”,Caatinga coral snake

■ ■

Micrurus lemniscatus (Linnaeus, 1758)—SouthAmerican coral snake

■ –a –a –a –a –a


Table 1 (continued)




Viperidae

Bothropoides erythromelas (Amaral, 1923) ■ –a

Bothropoides jararaca (Wied, 1824) ■ –a –a –a –a –a

Bothriopsis bilineata (Wied, 1825)—“surucucu-de-pindoba”, “pingo-de-ouro”, Two-striped forest pitviper

■ –a –a –a –a

Bothrops jararacussu Lacerda, 1884 ■ LC –a –a –a EN –a

Bothrops leucurus Wagler, 1824—“jararaca” ■ ■ –a –a –a

Caudisona durissa (Linnaeus, 1758)—“cascavel”,South American Rattlesnake

■ ■ ■ ■ ■ LC –a –a –a

Lachesis muta (Linnaeus, 1766)—“surucucupico-de-jaca”, Bushmaster

■ ■ ■ CR EN –a VU –a

Rhinocerophis alternatus (Duméril, Bibron &Duméril, 1854)

■ –a –a –a –a –a

CHELONIAN

Chelidae

Chelus fimbriatus (Schneider, 1783)—Matamata Turtle ■ ■ ■Mesoclemmys tuberculata (Lüderwaldt, 1926)—“cágado”, “cágado-d’água”,

■ ■ ■ –a

Mesoclemmys nasuta (Schweigger, 1812) ■ ■Platemys platycephala (Schneider, 1792)—Twisted-neck Turtle

■

Phrynops geoffroanus (Schweigger, 1812)—“cágado”,Geoffroy's Side-necked Turtle

■ ■ ■ ■ –a –a –a –a –a

Phrynops tuberosus (Peters, 1870)—“cágado”,Tuberculate Toad-headed Turtle

■ ■ ■ ■

Cheloniidae

Caretta caretta (Linnaeus, 1758)—“tartaruga cabeçuda”,loggerhead sea turtle

■ ■ ■ EN VU VU EN –a VU

Chelonia mydas (Linnaeus, 1758) “tartaruga verde”,“aruanã”, Green Sea Turtle

■ ■ ■ EN VU VU EN –a VU

Eretmochelys imbricata (Linnaeus, 1766)—“tartarugade pente”, hawksbill sea turtle

■ ■ ■ CR EN VU EN –a EN

Lepidochelys olivacea (Eschscholtz, 1829)—oliveridley sea turtle

■ ■ ■ VU EN EN –a EN

Dermochelyidae

Dermochelys coriacea (Linnaeus, 1766)—“tartarugade couro”, leatherback sea turtle

■ ■ ■ CR CR VU EN –a CR

Emydidae

Trachemys dorbigni (Duméril & Bibron, 1835)—Orbigny's Slider

■ –a

Geoemydidae

Rhinoclemmys punctularia (Daudin, 1801)—Spot-legged Turtle

■ ■ ■

Kinosternidae

Kinosternon scorpioides (Linnaeus, 1766)—“muçuã”,Scorpion Mud Turtle

■ ■ NT

Podocnemididae

Peltocephalus dumerilianus (Schweigger, 1812)—“cabeçuda”, big-headed Amazon River turtle

■ ■ ■ VU

Podocnemis erythrocephala (Spix, 1824)—Red-headed River Turtle

■ ■ VU

Podocnemis expansa (Schweigger, 1812)—“tartaruga da amazônia”, True Amazon Turtle

■ ■ ■ CD

Podocnemis sextuberculata Cornalia, 1849—Six-tubercled River Turtle

■ ■ ■ VU

Podocnemis unifilis Troschel, 1848—“tracajá”,Yellow-spotted River Turtle

■ ■ ■ ■

Testudinidae

Chelonoidis carbonaria (Spix, 1824) “jabuti” ■ ■ ■ ■ ■ –a –a EN –a –a


richness and abundance is higher. Numerous studieshave noted that Amazonian chelonians are widelyconsumed by local human populations and trans-formed into traditional regional commercial products(Smith 1976; Pezzuti et al. 2004; Rebêlo et al. 2005;Alves and Santana 2008; Pezzuti 2009; Pezzuti and

Chaves 2009). Klemens and Thorbjarnarson (1995)undertook a global study of the importance of reptilesin human diets and reported the presence ofchelonians as protein sources for both coastal andinland populations. In Brazil, freshwater turtlessuch as Podocnemis expansa (the Amazonian turtle)

Table 1 (continued)




Chelonoidis denticulata (Linnaeus, 1766) “jabuti” ■ ■ ■ ■ ■ VU –a –a –a –a –a

LIZARDS

Anguidae

Ophiodes striatus (Spix, 1825) ■ –a –a –a –a –a

Amphisbaenidae

Amphisbaena alba Linnaeus, 1758—Red Worm Lizard ■ LC –a –a –a –a –a

Amphisbaena polystega (Duméril, 1851)—BahiaWorm Lizard

■ LC –a

Amphisbaena vermicularis Wagler, 1824 ■ –a

Gekkonidae

Hemidactylus mabouia (Moreau de Jonnès, 1818)—“lagartixa”, “briba”, Afro-American House Gecko

■ –a –a –a –a –a

Iguanidae

Iguana iguana (Linnaeus, 1758) “camaleão”,“iguana”, Common Green Iguana

■ ■ ■ –a –a –a –a –a

Phyllodactylidae

Phyllopezus periosus Rodrigues, 1986—“briba” ■

Polychrotidae

Polychrus acutirostris Spix, 1825 ■ –a –a

Polychrus marmoratus (Linnaeus, 1758)—Many-coloredBush Anole

■ –a –a –a

Anolis fuscoauratus D’orbigny, 1837 ■ –a

Teiidae

Ameiva ameiva (Linnaeus, 1758)—“sardão grande”,“bico doce”, South American Ground Lizard

■ ■ –a –a

Cnemidophorus ocellifer (Spix, 1825)—“sardão pequeno”,“calanguinho”, “calango”

■ ■ –a –a

Dracaena guianensis Daudin, 1802 ■Tupinambis merianae (Duméril & Bibron, 1839)—“tegu”,“tejuaçú”, “teiú”, White tegu

■ ■ ■ ■ ■ LC –a –a VU –a –a

Tupinambis rufescens (Günther, 1871)—"teiú", Black Tegu ■ ■ –a –a

Tupinambis teguixin (Linnaeus, 1758)—"tejuaçú", lizard teju ■ ■ ■ ■ ■ –a –a –a –a

Tropiduridae

Tropidurus hispidus (Spix, 1825)—“lagartixa”, “catenga”,“catexa”

■ LC –a

Tropidurus semitaeniatus(Spix, 1825)—“lagartixa-de-lajedo”,Striped Lava Lizard

■ –a

Tropidurus torquatus (Wied, 1820)—“lagartixa” ■ –a –a –a –a –a

Uranoscodon superciliosus (Linnaeus, 1758)—“tamaquaré” ■ ■

TOTAL: 81 species 38 54 20 18 28 40 25 5 4 6 11 3 5

F food resource, M medicinal, MR magic/religious, P pets, O ornamentation and decoration, CR conflicting relationships. States: MGMinas Gerais, RJ Rio de Janeiro, SP São Paulo, RS Rio Grande do Sul, ES Espírito Santo; BR Brazil Red List (Brazil’s List ofEndangered Species); IUCN Red List categories (World Conservation Union; www.iucnredlist.org/): LC Least Concern, CDConservation dependent, CR Critically Endangered, EN Endangered, NT Near threatened, VU Vulnerablea States where a species occurs but does not figure in any red list


http://www.iucnredlist.org/

and Podocnemis unifilis (“tracajá”) are widely dis-tributed and sympatric in many regions of theAmazon basin and are widely eaten there.

The situation is no different for marine turtles,and all of the species that occur along the coast ofBrazil are used as food sources. On the northerncoast of Bahia State, for example, four species ofmarine turtles are eaten by indigenous coastalAmerindians. The Praia de Siribinha Beach, animportant area for turtle reproduction, was knownas a good place to capture these turtles, especiallywhen the females moved onto the shore to laytheir eggs (Costa-Neto 2001).

As hunting pressure increased along the Braziliancoast the sea turtles suffered very significant populationdeclines, and these reptiles were eventually listed asthreatened with extinction (Machado et al. 2008). Theconsumption of marine turtle meat and the use of theirshells to make eyeglass frames, combs, bracelets,rings, and necklaces, as well as the removal oftheir eggs for direct consumption, were commonoccurrences.

Sea turtles have a long history of exploitation inBrazil, practices that have contributed to a decline inthe abundance of the Brazilian species, implying thenecessity to adopt protective measures aimed at thesereptiles. Marine turtles are now protected by federallaws, however, and anyone caught killing them can bepunished with fixed prison sentences. Conservationactivities began in 1980, with the creation of theBrazilian Sea Turtle Conservation Program—ProjetoTAMAR-IBAMA. This project has been activelyinvolved in sea turtle conservation in Brazil for thepast 30 years and currently operates a network of 21research stations in 9 states distributed along1,100 km of coastline (Marcovaldi and Marcovaldi1999). The TAMAR project has worked intensivelywith fishers on the coast, for example, and part of thepopulation recovery of some turtle species canprobably be attributed to TAMAR's efforts, whichinclude environmental education and alternative sourcesof income for fishers in some villages withbeaches that are important for turtle reproduction(Marcovaldi and Marcovaldi 1999; Marcovaldi et al.2005; Suassuna 2005)

Chelonians are consumed as food throughout theworld (Balazs 1983; Allen 2007; Rudrud 2010) andmany traditional coastal communities still hunt marineturtles for their own subsistence and commercial

purposes. The Miskito Amerindians living along theeastern coast of Nicaragua, for example, dependentheavily on green sea turtles (Chelonia mydas). Thesereptiles supply them with meat, leather, fat (oil),shells, and “calipee” (a gelatinous substance foundinside the shell that is the basis of turtle soup;Nietschmann 1974). Marine turtles are revered onsome islands in the Pacific as sacred animals and servedas ceremonial food, and are more culturally valued thanother marine animals (Rudrud et al. 2007).

Chelonians as food in the Amazon region

Freshwater turtles had been an important food sourcefor the inhabitants of the Amazon region even beforethe arrival of European settlers, especially during thedry season. In a detailed narrative of a journey bySpanish explorers from Peru to the mouth of theAmazon and then back to the Old World, Carvajal(1955) described how thousands of chelonians weremaintained in wooden pens to supply fresh meat forthe large Indian settlements along the margins of themain course of the Amazon River.

…como habia gran cantidad de comida, ansi detortugas, em corrales y albergues de água, ymucha carne y pescado y biscocho, y esto tantoem abundancia, que había para comer un realde mil hombres un año… I teniendo recogidasmás de mil tortugas revuelven los indios unasegunda vez (Fray Gaspar de Carvajal, 1543)

After the arrival of colonists, this subsistenceactivity grew into a mercantile production system inwhich the main product was turtle egg oil (used forfrying food, boat caulking, medicinal purposes, and asfuel for public and domestic illumination). The largestbeaches along the Solimões–Amazonas Rivers andtheir major tributaries were established as RoyalTurtle Fisheries, and egg collection and oilproduction were rigorously controlled by thePortuguese Crown (Coutinho 1868; Bates 1892).The target species was the giant South American riverturtle, P. expansa (“tartaruga”), which nested inmassive numbers on the largest sandy beaches of theAmazon and its tributaries.

Gilmore (1986) suggested that harvesting the giantSouth American river turtle in the Amazon Basin washistorically the most important ethnozoological activityin the entire neotropical region. This activity has been


going on for at least 300 years, leading to drasticreductions in turtle populations throughout the AmazonBasin (Coutinho 1868; Bates 1892; Smith 1974;Mittermeier 1975; Johns 1987).

There is currently no large-scale commercialharvesting of freshwater turtles in the Amazon region,but they still constitute a significant food resource forhuman populations living along the rivers and aresold in local markets. Due to protective initiativesestablished at the beginning of the twentieth centuryturtle oil is no longer commercially sold, but theconsumption of adults and eggs continues (Smith1974). Populations of P. expansa were severelydepleted or even extirpated throughout most of itsformer distribution range (Fig. 1) and harvesting hasgradually become focused on other smaller podocne-mididae species such as P. unifilis (“tracajá”, Fig. 1),P. Podocnemis sextuberculata (“iaçá”, “pitiú”, Fig. 1),Podocnemis erythrocephala (“irapuca”, Fig. 2b), andPeltocephalus dumerilianus (“cabeçudo”, Fig. 2d,e),with some local variations between whitewater, clear-water, and blackwater subsystems (Smith 1974; Molland Moll 2004). The chelids Chelus fimbriatus(Fig. 1), Mesoclemmys gibba, Batrachemys raniceps,Batrachemys nasuta, Rhinemys rufipes, and Platemysplatycephala are not regularly consumed, and inmany places are actually the subjects of food taboos(Pezzuti et al. 2010a, b). The kinosternid Kinosternonscorpioides and the geoemidid Rhinoclemmys punc-tularia are consumed in the Amazon and Tocantinsdeltas, but the resulting impacts on local populationshave not yet been quantified (Smith 1974; Moll andMoll 2004). As mentioned above, the terrestrialchelonians Chelonoidis denticulata and Chelonoidiscarbonaria (Fig. 1) are eaten throughout theirdistribution ranges in South America. The observationthat some species of freshwater turtles are more oftenconsumed in some communities and rejected as foodin others is not surprising and is in agreement withMeyer-Rochow (2009), who stated that some animalspecies that seemed perfectly edible and suitable forconsumption by one ethnic group could be rejectedand banned by another.

Examples of ethnozoological events associatedwith the capture and consumption of chelonians inthe Amazon region is showed in Fig. 2.

Strong conservation initiatives were established inBrazil at the end of the 1970s, including the effectiveprotection of several important “tartaruga” nesting

beaches (Fig. 1). This led to one the development ofone of the largest turtle conservation projects in theworld coordinated by the Brazilian Federal Biodiversityand Conservation Agency (Instituto Chico Mendes paraConservação da Biodiversidade—ICMBIO). Agree-ments made between ICMBIO and local partners(mainly the administrators of small riverside towns inthe Amazon basin) guaranteed the survival of severallarge breeding populations of freshwater turtles byprotecting nesting sites and the deep river areas whereturtles tend to concentrate during the low-water season(Jul–Dec). Enforcement only occurs during the repro-ductive season, however, even in Conservation Areas,and is not sufficient to restrain subsistence use or thelarge web of illegal regional commerce (Cantarelli1997; Moll and Moll 2004).

Similar situations exist in the Trombetas BiologicalReserve on the Trombetas River (Alho and Pádua1982), the Abufari Biological Reserve on the PurusRiver (Kemenes and Pantoja-Lima 2006), the MadeiraRiver (Smith 1974), the Mamirauá Reserve on theSolimões River, the Jaú National Park on the NegroRiver (Rebêlo and Lugli 1996; Rebêlo and Pezzuti2000; Pezzuti et al. 2004; Rebêlo et al. 2006; Pezzutiet al. 2010a), the Mamirauá Sustainable DevelopmentReserve (Fachín-Terán et al. 2004), and the XinguRiver (Juarez Pezzuti, unpublished data). The mostcritical conservation factor is poaching breedingfemales during the egg-laying season.

Other important concerns for freshwater turtle con-servation and management in the Amazon Basin includethe effects of global warming and large-scale deforesta-tion on the hydrological cycle. Both factors can increasenest losses due to flooding (the major natural cause ofembryo mortality) throughout the Amazon Basin (Alhoand Pádua 1982; Mitchell and Quiñones 1994; Pezzutiand Vogt 1999; Batistella and Vogt 2008).

Caimans

Crocodylia composes the other important group ofreptiles harvested for food by traditional Braziliancommunities. Although only a few ethnozoologicalpublications have mentioned caimans as making uppart of human diets, it appears that essentially all ofthe caiman species that occur in Brazil are readilyeaten (Klemens and Thorbjarnarson 1995; Verdade2004; Alves and Rosa 2006, 2007a,b; Alves et al.2007b; Valsecchi and Amaral 2009).


Fig. 1 Examples of chelonians species used by human populations in Brazil


Lizards

There are published reports of at least seven lizardspecies being consumed by human populations in Brazil:Cnemidophorus ocellifer (Spix, 1825), Dracaenaguianensis Daudin 1802 (“lagarto-jacaré”), Ameivaameiva (“calango bico doce”), Tupinambis merianae

(“teiú”, “tejo”, “tejuaçú”), Tupinambis teguixin(“teiú”, “tejo”, “tejuaçú”, “jacuraru”), Tupinambisteguixin rufescens (“teiú”), and Iguana iguana(“sinimbú”, “camaleão”; Fig. 3). The last four speciesare the most commonly consumed lizards within theirnatural ranges in both Brazil and neighboringcountries. Fitzgerald (1994) reported that species ofthe genus Tupinambis are hunted for food inArgentina, Paraguay, and parts of Bolivia. The “teiú”is considered a delicacy, and its taste is oftencompared to chicken. The consumption and commer-cialization of I. iguana meat is very common in thetropical Americas (Klemens and Thorbjarnarson1995, Werner 1991), and its meat and eggs are theprincipal protein sources in many diets. In Brazil, theconsumption of “camaleões” and “teiús” has beenreported not just in rural areas but also in large urbancenters (Marques and Guerreiro 2007; Alves et al.2009a, b).

Both the meat and eggs of “camaleões” are widelyconsumed by members of traditional fishing commu-nities living on the Ilha do Marajó Island at the mouthof the Amazon River in Pará State (Alves RRN,personal observations), and specimens of I. iguanaand Tupinambis sp. were encountered being sold inthe public markets in the city of Feira de Santana,Bahia State (Marques and Guerreiro 2007). The greeniguana (I. iguana) has been a source of protein forhumans for over 7,000 years (Cooke 1981). Manyrural poor still depend on the Iguana for protein(Fitch et al. 1982). Iguana is consumed in all of thecountries within its distribution range, and iguanameat and eggs are considered to be aphrodisiacs anddelicacies in many areas. In Panama, an estimated70% of the population would consume iguana meatand eggs if they were available. Exact data on theextent of iguana consumption in other countries islacking (Werner 1991). The importance of iguanameat and eggs is evident, however, in the concernexpressed about their dwindling numbers and aboutthe resultant protein shortage for the social and ethnicgroups that depend on this protein source (Hirth 1963;Fitch et al. 1982; Ruiz and Rand 1985; Werner 1991).

Snakes

Only a few species of snakes have been reported asbeing eaten in Brazil, including Boa constrictor(“jibóia”), Eunectes murinus (“anaconda”, “sucuri”,

Fig. 2 Ethnozoological events associated with the capture andconsumption of chelonians in the Amazon region. a a woodenpen containing more than 2,000 turtles destined to be traded inTapauá City, Purus River, Abufari Biological Reserve; b turtlehunters with recently captured Mesoclemmys raniceps andPeltocephalus dumerilianus on the Carabinani River, JaúNational Park, Negro River; c 2,028 turtles, including Podoc-nemis expansa, P. unifilis and P. sextuberculata, apprehended inthe Abufari Biological Reserve, Purus River; d wild-caughtPeltocephalus dumerilianus destined to be traded in NegroRiver communities; e slaughtering large Peltocephalus dumer-ilianus turtles for food, Barcelos, Negro River; f next meal—aspecimen of Podocnemis erythrocephala recently captured by10-year-old children in Jaú National Park; g the skulls andshells of the peccaries and tortoises eaten by Araweté Indiansliving along the Ipixuna River, Xingu, Pará, northern Brazil


“cobra sucurijú”, “cobra grande”), Lachesis muta(“surucucu pico-de-jaca”), and Caudisona durissa(“cascavel”; Fig. 4). The consumption of B. constric-tor was reported by Fita et al. (2010) in the munici-pality of Santa Terezinha, Bahia State. Marques andGuerreiro (2007) reported that snake meat snackswere being sold for about US$1.50 in public marketsin Feira de Santana, Bahia—reflecting a custom thatis more common in southwestern regions of theUnited State and Mexico where rattlesnake meat(Crotalus spp.) is very popular and increasingly sold

in urban areas (Klemens and Thorbjarnarson 1995).Dried snake meat and snake meat powders areconsumed as a Mexican–American folk remedies(Bhatt et al. 1989), corroborating with Alves et al.(2007b) who noted that the consumption of reptiles isoften associated with folk medicine. The commercial-ization of snake meat in North America and in thesemi-arid region of northeastern Brazil indicates thatthis habit is not exclusive to southeastern Asia (as hadbeen suggested by Klemens and Thorbjarnarson(1995)).

Fig. 3 Some species oflizards used as food or formedicinal purposesin Brazil

Fig. 4 Some species ofsnakes used by humansand/or killed because theywere considereddangerous


The small numbers of snake species currently used asfood in Brazil is not surprising given the negative imagesattributed to these animals in myths, legends and popularbeliefs (Alves et al. 2010a). Rea (1981) noted that notonly snakes are rejected because of their disagreeablenature—but any other creature with a similar shape orbehavior will receive similar treatment. A studyundertaken among human populations living alongthe banks of the Rio Negro River (Amazonas State,Brazil) indicated that the electric eel (Electrophoruselectricus) was one of the least favored meats becauseof its strong smell and the shape of its body—“itlooks just like a snake” (Silva 2007)

Medicinal uses

Reptiles are one of the groups most closely associatedwith the history of medicine. The Greeks and Romansworshipped snakes and the god of medicine isrepresented holding a snake (which is supposed tobe Coluber sp., the so-called “Æsculapian snake”;Boulenger 2000). Various species of reptiles, espe-cially lizards and snakes, are used in the mostimportant traditional pharmacopoeias in the world(Alves et al. 2008). A recent review found that fivespecies of snakes, two lizards and a turtle are used inlocal traditional medicine in India (see Mahawar andJaroli 2008), a likely underestimate given the culturalrichness and size of that country. A more recent paperby Chakravorty et al. (2011) states that about 8% oftherapeutically used vertebrates among NortheastIndian tribes are reptiles. A powder made from geckos(Gekko gecko [Linnaeus, 1758]) is used in traditionalChinese medicine for humidifying the lungs and totreat asthma, and the shell of Chinese softshell turtle(Pelodiscus sinensis [Wiegmann, 1834]) is prescribedfor softening and removing lumps (Wu 2005).

Analyses of historical documents indicated thatreptiles were used in traditional medicines in Brazilduring pre-colonial times (Silva et al. 2004; Almeidaet al. 2005; Alves et al. 2007b). For example, duringhis voyage through the interior of Brazil in thenineteenth century, Von Martius (1939) recordedmany natural medicines being used by the Amerindiantribes he encountered, such as fresh caiman fat appliedto alleviate rheumatism (Costa-Neto 2005). Even today,caiman fat (Cayman latirostris, Melanosuchus niger,and Paleosuchus palpebrosus) is used in rural andurban communities to treat rheumatism (Alves and

Rosa 2006, 2007a, 2010; Alves et al. 2007b).Examples of reptiles that have been used in Brazilsince colonial times include: I. iguana, Caimanlatirostris, C. durissa, and Micrurus ibiboboca (Alveset al. 2009a).

A total of 54 species of reptiles are used formedicinal purposes in Brazil. This number represent15.38% of medicinal animals recorded in Brazil(Alves 2009; Alves and Alves 2011; Alves et al.2007a,b; Costa-Neto and Alves 2010) and demon-strates the importance of this animal group in Brazilianzootherapeutical practices. Reptiles are used to treatapproximately 100 illnesses in Brazil. Thirty-fourspecies have multiple therapeutic uses and are pre-scribed to treat various diseases, and different reptilescan often be used to treat the same illnesses. Productsderived from T. merianae and T. teguixin, for example,were indicated for treating 8 and 18 conditionsrespectively, and medicinal products derived from E.murinus were cited as being useful in treatingwounds, skin problems, bruises, sprains, arthrosis,rheumatism, boils, sexual impotence, headache, sorethroat, thrombosis, swelling, tumors, asthma, musclestrains, numbness, syphilis, and for reducing pain andbruising (Alves et al. 2007b; 2010c).

Different methods of preparing and administeringanimal remedies have been recorded in Braziliantraditional medicine. Hard parts, such as bones, rattlesand snake skins are generally sun-dried, grated,crushed to a powder and then administered in teasor eaten during meals; fats and oils are either ingesteddirectly or used as ointments (according to diseasebeing treated (Alves and Rosa 2006; Alves et al.2007b). Examples of products derived from reptilesused medicinal or magic religious purposes is shownin Figs. 5, 6, 7. Additional details on reptile parts usedas medicine, conditions treated with the remedy andways of administration are available in Alves et al.(2009a, b).

Human societies often develop elaborate culturalbeliefs, values, and customs regarding wildlife.Besides their role in healing, natural products alsofrequently take on a magical–religious significance,reflecting the different views of health and diseasethat exist within different cultures. Traditional Brazilianhealing is intertwined with cultural and religious beliefsand is holistic in nature. The influence of magical beliefsintegrated into traditional medicine is apparent in Brazil,and zootherapeutic practices are closely connected with


Afro-Brazilian religions (which have also incorporatedelements from indigenous peoples). Reptiles areemployed within a magical-prophylactic perspective,with the purpose of warding off diseases of “unnatural”origin—a practice that encompasses the perception thatsupernatural forces are involved in causing diseases, as

well as in their treatment. In this context, animal partsare used to prepare clinical remedies as well as to makeamulets or charms used in magical/religious diagnoses.Popular beliefs usually affect the way species are used inzootherapy (Alves and Rosa 2006). One form ofspiritual treatment involves the use of amulets

Fig. 5 Examples ofproducts derived fromreptiles commercialized inBrazilian cities for medici-nal or magic religious pur-poses. a a live “Jiboia” (Boaconstrictor) kept in a shopselling magic/religiousarticles in order to commer-cialize its feces; b “Patuá”made from “Jiboia” leather:c Head and fat of a “Jiboia”and the rattle and fat from arattlesnake (Caudisona dur-issa) and; d “Jabuti” turtleheads (C. denticulata (left)and C. carbonaria (right))

Fig. 6 “Águas” (waters) orperfumes derived from rep-tiles (a Boa constrictor, bSpilotes pullatus, c Iguanaiguana, d Uranoscodonsuperciliosus (photos:Rômulo Alves)


containing reptile parts to protect the user from the “evil-eye” or from diseases (Alves and Pereira Filho 2007).Caiman teeth (C. latirostris, M. niger, and P.palpebrosus), for example, are used as protectionagainst snake bites (Costa-Neto 2005; Alves et al.2007b).

Magic religious uses

A variety of wild animals are integral parts of culturaland religious festivals and ceremonies, some of whichwas designed to promote human health (Ajayi 1978),and certain species may be sacrificed during therituals and festivities (Adeola 1992). Reptiles arecommonly associated with myths in differentcountries and are commonly used in magic–religiousrituals. A good example is the serpent cult that stillpersists in India, central Africa, Oceania, Greece,Egypt, Rome, and in the east. These peoplevenerate serpents and snake-like gods as protectors,representatives of fecundity, terrestrial creativeforces, holders of hermetic secrets, and as symbolsof the infinite (biting their own tails; Biedermann1996). Images of serpents are common throughout theworld, and in equatorial Africa (Congo to Cameroon)serpent take the form of wise, guiding forest spirits(Cascudo 1962).

At least 20 reptile species have been recorded ashaving magic–religious uses in Brazil (Alves 2006b;Alves and Pereira Filho 2007; Alves 2008; Léo Netoet al. 2009), and reptiles are commonly sold inoutdoor markets and stores that also sell religiousarticles. Reptile products are widely used by Afro-Brazilian religious followers. The animals are occa-sionally sold whole, but mostly cut into pieces (flesh,skin, tails, eyes, heads, teeth, cloacae, fat, rattles,carapaces) with a single reptile providing manydifferent raw materials (Alves 2006b; Alves andPereira Filho 2007, Léo Neto and Alves 2010). Somemagical–religious reptile uses recorded in Brazil aresimilar to those seen in Africa, clearly reflecting aninherited African influence. Animal products are usedin cultural ceremonies (e.g., during funerals or whenleaders take office) and traditional rites (e.g., toinvoke the Gods or to reconcile with them), and havea very significant role in the traditional pharmaco-poeia in the dry regions of Nigeria (Adeola 1992).Sodeinde and Soewu (1999) reported that animals andtheir parts are used in Nigeria as charms forameliorating/treating certain problems. The wholebody of the Senegal Chameleon (Chamaeleo senegal-ensis), for example, is used to make its ownerinvincible to detractors or to other charms. In SouthAfrica, traditional healers use snake skins as magiccharms to assure health and success (Lugira 2009).

Fig. 7 Examples of the useof reptiles. Tupinambismerianae killed to be eaten(a) and subsequently stuffedto be used as an ornament(b), Iguana iguana beingroasted for subsequentmedicinal use (c), and arattlesnake rattle used forsimilar purposes (d)


Reptiles and their parts also are used in sacrifices toappease and invoke spirits and traditional gods; thehead of P. sebae (African Python), for example, isused to invoke and protect against witches. In Brazil,the head of another Boidae (B. constrictor) is used forsimilar purposes (Alves et al. 2009a; 2010a).

In addition to whole animals or their parts, otherproducts derived from reptiles are offered for sale inBrazilian cities, principally “águas” (waters) orperfumes (Fig. 6) and “pó” (powder). The águas orperfumes are products that contain reptiles suspendedin ingredients such as alcohol, rose water, or solutionswith other plant materials. The “waters” or “perfumes”are mixed with water during baths or utilized as aperfume following the bath. It is believed that thisprocedure will make the bath user achieve love andfinancial success (Alves and Pereira Filho 2007; Alveset al. 2009a; 2010a). The pó is produced from theanimals or their parts that are dried in the sun and thenground to a fine powder with a mortar and pestle.Reptile species utilized for the preparation of “waters”or “perfumes” and pó (“powder”) are B. constrictor, I.iguana, Uranoscodon superciliosus, C. denticulata,and C. carbonaria.

Reptiles that move slowly (“lerdos”) are used tocalm people (“lerdar”). For example, the productsproduced from U. superciliosus (dust and water) areused to “amansar” (to calm an aggressive person orease the anger of someone betrayed by their wife orhusband). There is an association between thebiological characteristics of a lizard and the effectsits use is expected to generate (Alves 2006b, 2008).This observation is similar to that of Radbill (1976)who pointed out that in homeopathic or imitativemagic it is assumed that certain qualities attributed toanimals can be transferred to humans, and that thistransfer can occur by inhalation, ingestion or applicationof the body parts of those animals.

Another product derived from reptiles and verypopular in stores are “patuás” (Fig. 6), a kind ofamulet that is hung around the neck, glued on a pieceof cloth or kept in a pocket or wallet. They are squareor round pouches, usually made of leather or somesynthetic material, made to hold animal parts (piecesof snake skin or dolphins’ eyes; Alves and Rosa2008). According to the owners of shops in which thismaterial is sold, these amulets are very popular amongcustomers seeking good luck, love, and financialsuccess (Alves 2006b; Alves and Pereira Filho 2007).

There is a great deal of overlap in species use as thesame animal can be used for multiple magical religiouspurposes. Different parts ofB. constrictor, for example,can be sold: skin, tails, cloacae, eyes, heads, excre-ment, fat, and teeth. “Águas” and “pó” can also bemade with the heads or bodies, and these productshave various indications, such as success in love, withmoney, with gambling, travel, and business dealings(Alves 2006b; Alves and Pereira Filho 2007).

Reptiles as pets

The great variety of animals kept as pets throughoutthe world include not only innumerable mammals,birds and fish, but also reptiles and amphibians(Franke and Telecky 2001; Jepson and Ladle 2005;Alves et al. 2010b), and global demand has increasedsignificantly in recent decades. Hoover (1998) notedthat reptiles are being widely commercialized due totheir relative abundance, the wide variety of speciesthat can be acquired, the development of bettertechniques for raising them in captivity, the growth ofrestrictions on the commercialization of other species ofanimals and, principally, because of the fact that theygenerally require less care than mammals or birds.

At least 18 reptile species are sold as pets in Brazil,especially chelonians (seven species, 41.17%), butalso snakes (e.g., B. constrictor) and lizards such asT. merianeae (“teiú”) and I. iguana (“camaleão”;Fig. 3).

Among the chelonians sold or kept as pets are twopopular species (C. carbonaria and C. denticulata;Fig. 1). These animals are relatively docile, easy tocapture and take care of; there is also a popular beliefthat their presence helps avoid illnesses such asbronchitis and asthma (Alves et al. 2009a). Accordingto Fitzgerald (1989) and Lopes (1991), Chelonoidissp. is the most frequently commercialized reptile inBrazil (and in the world), being widely sold to petshops, private collectors, and zoos.

Among the reptiles most frequently abandoned byprivate collectors and donated to the Center for theConservation and Management of Reptiles andAmphibians (RAN) in Goiânia, Goiás State, are:Trachemys scripta (the red-eared slider), an exoticspecies from southern United States, and Trachemysdorbigni (“tigre d’água Brasileiro”), which is endemicto Rio Grande do Sul State (Souza et al. 2008). Bothspecies are highly sought after as pets, although their


trade is largely illicit. They are usually sold when just4 or 5 cm long, although they can reach up to 30 cmas adults. The former species is most widely soldthroughout Brazil (even though its importation hasbeen prohibited since 1991), while the latter species isendemic to Rio Grande do Sul State (but has sincebeen disseminated to many other parts of the country;Souza et al. 2008).

Among the snakes most widely preferred as petsare species of the family Boidae, principally the“jibóia” (B. constrictor)—this is probably related tothe fact that they are not venomous and offer littledanger when handled. Poisonous snakes are kept aspets as well, but much less frequently. Among thelizards the most widely preferred as pets are I. iguanaand Tupinambis spp. Souza et al. (2008) noted thatkeeping poisonous snakes at home offers serious risksof being bitten—and perhaps by a snake for whichthere is no specific anti-venom available in Brazil.Caimans are also occasionally raised as pets,principally when they are young, but this groupis not at all as commonly kept as are lizards,chelonians, and non-poisonous snakes.

Most of the specimens kept as pets in Brazil areacquired on the black market, and are thereforeillegal. Additionally, the sale of illegal wild animalsgenerates secondary problems when their ownerswish to be rid of them (for fear of punishment,because of sentiments of guilt, or simply because theyno longer wish to care for these animals). Generally,these owners take one of two courses: (1) donatingthe animal to an institution that can take can care of itor return it to a secure natural environment, or (2)abandoning them anywhere at all, without any realconcern for their welfare (Souza et al. 2008).

Indiscriminately releasing these animals can createserious ecological problems, especially if they arenon-native species. The introduction of exotic species(such as the red-eared slider, T. scripta), can causesignificant harm to the local biota by: (1) competingfor food with native species, (2) preying on nativespecies (tadpoles and small fish and invertebrates, forexample), (3) hybridizing with other species of thesame genus, and (4) introducing parasites and/ordiseases. Any of these factors can result in seriousdisequilibriums of local ecosystems (Ribeiro andSousa 2004).

Another problem is related to the stress theseanimals experience during capture, transport, arrival

in a new environment, diet changes, and exposition inpet shops—often resulting in the loss of theirimmunological capacity and the subsequent onset ofillnesses. Reptiles are generally asymptomatic carriersof Salmonella spp., but infectious processes can beactivated under situations of stress with the consequentelimination of these bacteria in their feces. Oncereleased by infected animals, Salmonella demonstrateshigh persistence in natural environments, and directcontact with these animals or just secondary contactwith the localities where they were kept can causeinfections in humans (Grespan 2001; Fornazari andTeixeira 2009).

Reptiles as dangers to traditional human populations

Animals that represent real or supposed direct dangersto humans, such as large carnivores and reptiles, areoften killed for safety reasons (Fitter 1986), and of allthese animals, reptiles tend to be group mostfrequently considered dangerous and persecuted. Atthe same time that reptiles can have great utilitarianvalue to traditional communities, they are alsopotentially dangerous or harmful animals and areoften culturally associated with evil (Alves et al.2009b; 2010a). Thus, a reptile may be killed becauseit is considered harmful, but its sub-products willusually not be wasted. A good example of thissituation can be seen with “teiús” lizards (T. merianaeor T. teguixin), which are often killed because they eatchicken eggs or chicks—but their resources are usedas food, in ornamentation and popular medicine(Alves and Rosa 2006; Alves et al. 2009a; 2010aConfessor et al. 2009; Ferreira et al. 2009).

Poisonous snakes such as rattlesnakes (C. durrisa),coral snakes (Micrurus sp.), and vipers (Bothropoidesleucurus) are usually killed preventively as they canbite people or domestic animals (Alves et al. 2009b);but their body parts (fat and the rattle) are widely usedin home remedies (Alves and Rosa 2006). In aresearch project carried out in Mato Grosso State,Brazil, Trinca and Ferrari (2006) reported that somelocal hunters would be in favor of exterminating anyand all predators that might attack humans or theirdomestic animals—even if these predators were livingin their natural environment far from any normalcontact with human societies. This view reinforces thefact that many people believe that all snakes aredangerous and aggressive (Marcum 2007).


Prokop and Tunnicliffe (2008) and Prokopt et al.(2009) proposed that avoiding animals associatedwith danger can enter into conflict with the humantendency to favor rare animals. This hypothesis suggeststhat acquiring factual knowledge about animals willresult in more positive attitudes only if those animals arenot perceived as dangerous. Because reptiles have beenassociated with danger throughout evolution, Ohman andMineka (2003) proposed that it is likely that snakesrepresent a prototypical stimulus for activating a fearresponse. This is in agreement with Herzog et al.(1988), who proposed that evolutionary pressures areresponsible for human attitudes to animals. Inaddition, these authors proposed that human attitudesare also influenced by rarity and the populationdistributions of animals and are more favorablydisposed toward rare animals.

Even though many people know that not all snakesare dangerous, it is still common to refer to them withpejorative words such as ugly, repugnant, repulsive,cruel, treacherous, vicious, revengeful, offensive, etc.(Araújo 1978)—terms used to designate negativeattitudes or personality traits in humans. Researchundertaken in the semi-arid region of Paraíba State byAlves et al. (2009b) found that local residents killednot only venomous snakes but also non-venomousindividuals—because these animals provoked fearand repugnance, or simply because these peoplebelieve that all snakes are in some way potentiallydangerous. In Brazil, work undertaken in themunicipality of Santa Terezinha, Bahia State byFita et al. (2010) indicated that local residents havestrong negative reactions to snakes and kill themwhenever possible. Most people likewise customarilyconsider amphisbaenids as being snakes because theyare very similar in appearance.

One logical explanation for this great antipathytowards snakes lies in the force of myths associatedwith serpents that feed the natural fears people haveof these animals. Many societies have legends, fables,and stories in which serpents appear as astute animalswith bad intentions (Vainer 1945). These narrativesare almost always the fruit of incorrect interpretationsof snake behavior, but they remain fixed in thepopular imagination through generations, and arealmost impossible to erase (Alves et al. 2010a).Snakes have been symbols of hostility in manyhuman societies throughout the ages, due in part totheir perceived deceit of Adam and Eve in the biblical

Garden of Eden, as well as to a general lack ofknowledge and appreciation of snake biology andbehavior. These myths have resulted in the attributionof supernatural powers to snakes and largely portraythem in a negative light. Attuquayefio (2004) suggestthat the myth “all snakes are venomous and dangerous”may have originated from the perceived biblicaltreachery of snakes and the general belief that snakesare out to implement their “diabolical” plans to wipe thehuman race from the face of the earth. From thispremise, there is every justification for the belief that allsnakes are equipped with weapons (fangs and venom)with which to attack and kill any human being on sight.

This situation is sometimes mitigated by theexistence of legends that portray snakes as other thanstrictly malignant animals (Alves et al. 2010a).Because of the periodic changing of their skins,snakes symbolize health and a new beginning forsome cultures and their presence in human habitationsis interpreted as a good omen and an augury of thearrival of happiness (Santos 1987). Seen in a positivelight, snakes have been considered religious symbolsand repositories of fertility, wisdom, and good luck.Ancient Mexican Aztecs worshipped a mythicalfeathered serpent, Quetzalcoatl, as a fertility god and“master of life”. Many Amerindian societies regardsnakes as sacred because they are considered asreincarnations of important people (Nagas) (Carr1963; Jackson and Mirick 1996). In some parts ofAfrica, snakes are associated with the rainbow, andhave the power to control rainfall and rivers(Cansdale 1955).

Understanding the structure of a people’s mythsand fears might result in more successful pro-environmental actions (Prokop et al. 2009). The badreputations that reptiles (mainly snakes) have arerooted in stories and myths, so that combating mythscould result in effective improvements of humanattitudes towards all reptiles. Such efforts shouldinclude reaching out to science/biology teachers andstudents enrolling in biology courses, as it has beenobserved that their beliefs are not very different fromthose of non-biology students (Prokop et al. 2009).

Negative attitudes are not restricted just to snakes,and lizards are often considered venomous or disease-causing. In Northeast Brazil, the lizard Hemidactylus,for example, is considered venomous or a cause ofdermatological problems by populations. Ceríaco(2010) reported that folklore surrounding geckos is


very common and diverse in countries where thisanimal exists, but sometimes with completely oppo-site points of view. On Mindanao, in the PhilippineIslands, the inhabitants hesitate to live in detachedhuts where there are no geckos, for they believe that ifgeckos are not present something must be wrong withthe hut. In Thailand, on the other hand, people do notwant geckos in their homes because they believegeckos bring bad luck (Crump 2002).

Myths about geckos in Brazil may have originatedwith the Portuguese colonists. Ceríaco (2010) andCeríaco et al. (2011) pointed out that in Portugal geckosare considered poisonous. Many people are afraid totouch a gecko or even come in contact with a placewhere one has been. This apprehension is principallyfound in stories about someone being poisoned by agecko. One of the most common stories is about a geckofalling into a pot (or some other kitchen item) used forpreparing meals—if not washed in time, the peopleeating the food will either die or be severely poisoned.

Many reptiles are killed because they are consideredpotentially dangerous—and a total of 40 species ofBrazilian caimans, snakes and lizards have beenidentified as being frequently slaughtered for this motive(see Marques 1995; Alves et al. 2009b; Fita et al.2010). These observations reinforce the view ofMarques (1995) that the links between humans andthe zoological universe are full of contradictions andambiguities—because the native fauna is a source ofimportant resources but also harbors dark risks formen and their domestic animals. Conflicts betweenpeople and animals are not, of course, restricted toreptiles, and can involve other groups such ascarnivorous mammals (Conover 2002; Graham et al.2005; Marshall et al. 2007; Alves et al. 2009b; Inskipand Zimmermann 2009). Conflicts arise when thenecessities and behaviors of animals enter intoconflict with the objectives of human beings (damagingharvests, wounding or killing domestic animals,and/or threatening or killing humans), or when theneeds of humans generate negative impacts forwildlife (Kaltenborn et al. 2006; Treves et al. 2006).Conflicting interactions between wild life and humancommunities are extremely important in a conserva-tionist perspective, and represent a significant challengefor conservation managers who must try to benefit bothparties involved.

In addition to its direct impact on individuals andspecies, the consumption of reptiles can also spread

diseases that affect both people and wildlife. Numerousinfectious diseases, i.e., zoonoses, can be transmittedfrom animals to humans. The consumption of reptilemeat and other reptile products for medicinal purposesoccurs throughout the world and probably involvesbiological risks comparable to the consumption of anyother wild animal meat. These hazards includepathogenic agents within the meat or in other sub-products (including the reptilian digestive tract) orcontamination from contact with cutting surfacesor the meat from other species during slaughtering,butchering and processing. Although relativelyinfrequent, reports of food poisoning from reptileproducts indicate that their disease potential islikely to increase as consumption of these productsbecomes more common (Magnino et al. 2009).

Conservation implications

Our review demonstrated that 81 reptile species areused by human populations in Brazil for a variety ofdifferent purposes, and of these, 30 (37%) areincluded in endangered species lists. Many speciesare killed for their commercial value or simplybecause they are considered harmful, and the impactsof these relationships between humans and reptilesmust be taken into consideration when implementingrecovery plans for these animals (especially thosespecies that are intensively used).

Although hunting for reptiles is often associatedwith their utilitarian value, large numbers of reptiles(at least 40 species) are killed simply because they areconsidered “dangerous”—with snakes being thegroup most impacted by this outlook. This is notsurprising given that most human societies areophidiophobic due to their perception that snakes arevicious and cunning creatures with a deep hatred forhumans. All over the world and throughout recordedhistory, snakes have been a source of fascination andfear and they have been both worshipped anddespised. Snakes have featured prominently in thecustoms, religions, and folklore of human societiesthroughout the world, being held in high esteem bysome societies as untouchable gods or spirits, and inothers as evil, deadly, and despicable creatures withmagical, almost supernatural attributes (Attuquayefio2004; Alves et al. 2010a).

The contrasting useful/aesthetic and negative viewsabout certain animals constitute a significant problem


for biodiversity conservation programs and it willalways be necessary to take into consideration thecultural, economic, political and social characteristicsof the region when planning conservation activities(Meffe et al. 1997; Primack 2006). Jacobson and Duff(1998) pointed out, however, that most conservation-ists are not prepared (either personally or academi-cally) to adopt a holistic approach to this problem. Itis of vital importance to understand how people relateto the biodiversity that surrounds them in order to beable to develop successful programs of biodiversityconservation.

The manner in which natural resources are used byhuman populations and the cultural norms associatedwith those uses are extremely relevant to definingconservation strategies (Alves et al. 2008). As wehave seen in this review, there are many forms ofinteraction between reptiles and humans in Brazil—although most of them are quite negative in terms ofwildlife conservation—which reinforces the impor-tance of understanding such uses and interactions inthe context of protecting reptiles in Brazil.

Ultimately, the most successful conservation pro-grams are those that identify and correct the factorsthat endanger species while providing economicbenefits to local people (Pough et al. 2004). As such,what are the possible strategies of reptile managementand conservation that can minimize the impact of thehuman use? One option would be to create coopera-tives of reptile breeders to supply products derivedreptiles for different purposes. These cooperativescould exploit breeding sites of species such as P.expansa, P. unifilis, C. mydas, C. denticulata, C.carbonaria, T. merianae, P. palpebrosus, P. trigona-tus, B. constrictor, U. superciliosus, Tupinambis spp.,under the appropriate authorization and supervision ofgovernmental authorities and wildlife specialists(biologists, veterinarians and zootechnicians).

Sustainable-use programs for reptiles have hadsome success in the world (Vitt and Caldwell 2009;Pough et al. 2004), such as the snake collectors whoextract venom in India (Whitaker 1989). Lizards(Tupinambis, and certain iguanids) are harvested forlocal consumption and have experienced sharp popula-tion declines in many areas due to overhunting (Vitt andCaldwell 2009). Conservation strategies involvingsustainable use have to take into account bothbiological and socio-economic factors (Westing1996). Several studies have shown that socio-

economic sustainability can be achieved throughcommunity-based management plans. For instance,in the case of the olive ridley sea turtles at Ostional,Costa Rica [reviewed by Campbell (1998) andThorbjarnarson et al. (2000)], a successful conserva-tion program was carried out through a controllednest-predation project based on the exploitation ofnests that would otherwise be lost due to naturalcauses (Caputo et al. 2005).

Breeding programs to raise iguanas for release intothe wild have been developed in several countries,including Panama, Costa Rica, Guatemala, Nicaragua,Belize, Honduras, El Salvador, Colombia, andVenezuela (Eilers et al. 2002), and iguana farminghas become an attractive economical alternative tocattle breeding and a significant source of food forlocal populations (Magnino et al. 2009). Managedharvests of crocodilians began about three decadesago to assist the recovery of species and populationsthat had been devastated by unregulated hunting. Thesuccess of managed harvests and captive rearing inPapua New Guinea, Venezuela, and a few othercountries stimulated other governments to beginsimilar programs. These managed species haveshown a remarkable resilience in many countriesand their populations are no longer endangered.However, with more countries producing skins,supply began to exceed demand and was followedby a declining popularity for crocodylian leather(Vitt and Caldwell 2009).

Educational programs are also viable alternativeswhen focused on rural communities that eat reptilesand use them in traditional medicine and religiouspractices. Projects that train school teachers in thosecommunities and the old hunters’ train in sites nearprotected areas help minimize impacts on thesereptiles (Alves et al. 2010a). As pointed out by Poughet al. (2004), human education is urgently needed atall levels to help maintain viable populations ofreptiles. Training in areas such as habitat protection,wildlife management, and conservation biology isneeded—especially in tropical countries where mostreptile species are found. The success of conservationand management programs ultimately depends onhow well these programs are tailored to the interestsand needs of the people where the threatened and/orendangered animals live. Moura et al. (2010) pointedout that people with lower educational levels weremore likely to consider all snakes as dangerous, and


they also proved to be more hostile to these animals.More contact with scientific and environmentaleducation activities seems to have been decisive forthe higher tolerance to snakes. The implementation ofactivities of environmental education can increase theawareness of the importance of snakes, instructingthose who still consider them intrinsically harmful.

People will develop either positive or negativeattitudes about reptiles depending on the culturalbiases to which they are exposed, and these culturalbiases will affect whether or not these animals areconsidered worthy of protection (Campbell andCampbell 2001; snakes being the best example).Given the well-entrenched human fear (sometimeswarranted, and apparently evolutionarily explicable),radical action may be the only hope for snakeconservation. Saving snakes may require the rein-statement of reverence toward them, as is seen inmany indigenous societies around the world (i.e.,India, Africa, and Australia). Scientists are trained tobe objective and often view themselves as removedfrom religious and spiritual values, but understandingthe structure of peoples’ beliefs will surely result inmore successful pro-environmental actions. Theseefforts must include reaching out to science/biologyteachers and students enrolling in biology courses astheir beliefs in myths have been found to be similar tothose of non-biology students (Prokop et al. 2009).Alves et al. (2010d, e) pointed that under somecircumstances folk beliefs, religious doctrines andspecies-specific taboos can be important to theconservation of declining or threatened species andsuch positive practices should be stimulated. Additionalmeasures not directly involving behavior modificationof the local populations, such as controlling illegalwildlife trade, should likewise be considered.

The conservation of reptiles is more difficult thanother vertebrate groups owing to their generally badreputations in many regions of the world (Burghardtet al. 2009) and support for these programs iscertainly much more problematic than those involvingcharismatic animals like eagles or large carnivores(Martín-López et al. 2007). While it is true that thegreatest threats to reptiles and amphibians are habitatdestruction, pollution, climate change, and competitionwith alien species (Vitt and Caldwell 2009; Pough et al.2004), their complex relationships with humans (oftenresulting in their persecution, capture, and killing)represent serious and real threats (Alves et al. 2008,

2010a; Ceríaco 2010). Gibbons et al. (2000) pointedout that the use of reptiles is an integral part of manycultures. The great diversity of interactions betweenhumans and reptiles provide the foundations for thecultural, economic, emotional, intellectual, social, andspiritual motivations that will determine how conser-vation and management activities are designed, con-ducted, and assessed (Frazier 2005; Alves et al. 2008,2009a). Hence, an understanding of the cultural,social, and traditional role of these reptiles isfundamental to establishing management plans direct-ed towards their sustainable use. However, becausethis type of information is widely dispersed, and theeffects of different types of human-reptile interactionshave rarely been evaluated in a systematic way, thisissue will require much more attention in the nearfuture (Alves et al. 2009a; 2010a)

Acknowledgments To UEPB, UFPB, UFRN, UFPA, andURCA for all the support. The first author would like toacknowledge to CNPq (Conselho Nacional de DesenvolvimentoCientífico e Tecnológico) for providing a research fellowship.

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A review on human attitudes towards reptiles in Brazil

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