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Journal of Ethnopharmacology 130 (2010) 5460

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Journal of Ethnopharmacology
journal homepage: www.elsevier.com/locate/jethpharm

Ethnopharmacological Communication

The medicinal animal markets in the metropolitan region of Natal City, northeastern Brazil
Eduardo S. Oliveira a , Denise F. Torres a , Sharon E. Brooks b , Rmulo R.N. Alves c,
a

Universidade Federal do Rio Grande do Norte, Centro de Biocincias, 59072-900 Natal-RN, Brazil University of Cambridge, Department of Geography, CB2 3EN, UK c Universidade Estadual da Paraba, Av. das Baranas, 351/Campus Universitrio, Bodocong, 58109-753 Campina Grande-PB, Brazil
b

a r t i c l e

i n f o

a b s t r a c t
Aim of the study: This study investigates the trade of animals for medicinal purposes in Natal metropolitan area, northeastern Brazil, to document which animal species are used, how and for what purposes. This study also discusses the implications of the use of zootherapeutics for wildlife conservation. Materials and methods: Based on interviews with merchants of medicinal animals in all open fairs of the metropolitan region of Natal City, we calculated the informant consensus factor (ICF) to determine the consensus over which species are effective for particular ailments, as well as the species relative importance to determine the extent of potential utilization of each species. Results: We describe the therapeutic effects of 23 animal species used medicinally. The zootherapeutical products sold commercially are used to treat 34 health problems that were classied into 14 broad categories. We also highlight those species valued for their effectiveness against a range of ailments. The highest ICF value (1.0) was cited for diseases of the circulatory system, which include relief of symptoms such as stroke, hemorrhage, varicose veins and edema. Discussion and conclusion: Our study indicated that the local population holds a great deal of ethnomedical knowledge about their local animal resources, and highlights the need for clinical investigations of these traditional remedies to test the safety and efcacy. The animal species identied in this study not only hold high medicinal value for local populations, but could potentially be a source of healing compounds that could aid pharmaceutical research. While the impact of these practices on animal populations is unknown, the high extractive value of these animal populations and the associated medicinal traditional knowledge, needs to be considered in any conservation strategy aimed at the faunistic resources of this area. 2010 Elsevier Ireland Ltd. All rights reserved.

Article history: Received 22 December 2009 Received in revised form 4 April 2010 Accepted 6 April 2010 Available online 9 May 2010 Keywords: Ethnozoology Medicinal animals Zootherapy Traditional medicine

1. Introduction Traditional medicine based on animals and their products is of high importance to urban and rural livelihoods in Brazil (Alves et al., 2007a; Alves, 2009; Coutinho et al., 2009), and many animal species are sold in markets throughout the country (Freire, 1996; Costa-Neto, 1999; Almeida and Albuquerque, 2002; Silva et al., 2004; Alves and Santana, 2008; Alves et al., 2010a). Ethnozoological studies often involve market surveys for documenting animal species used and the traditional knowledge associated with that use (Alves and Rosa, 2007a). The markets, where traders of traditional medicine operate, represent important sales point for native and exotic fauna. According to Almeida and Albuquerque (2002), information on exotic and native ora and fauna obtained in these markets can provide the informa-

Corresponding author. Tel.: +55 83 32167775; fax: +55 83 32167775. E-mail address: romulo nobrega@yahoo.com.br (R.R.N. Alves). 0378-8741/$ see front matter 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.jep.2010.04.010

tion necessary for conservation strategies for commercialized resources. Given the increasing need for the conservation of wild animal species, coupled with the high value that many species hold for traditional medicine as well as potential drug discoveries by pharmaceutical industries, there is an urgent need to examine the ecological, cultural, social, and public health implications associated with fauna usage. This includes a full inventory of the animal species used for medicinal purposes and the socio-cultural context associated with their consumption (Alves et al., 2007a, 2010b,c). While the connections between traditional botanical remedies and conventional medicine in urban settings have been explored in recent publications (e.g., Balick et al., 2000, 2003; Williams et al., 2000; Maca et al., 2005; Albuquerque et al., 2007), there is a dearth of information on the use of animals as medicine by city dwellers (Alves and Rosa, 2007a; Alves and Santana, 2008; Alves et al., 2007a, 2010a). This study aims to understand the use of animal species in traditional medicine, based on a case study in Natal metropolitan area,

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E.S. Oliveira et al. / Journal of Ethnopharmacology 130 (2010) 5460 55

northeastern Brazil. In particular, we aim to document which animal species are used, how and for what purposes, to assess whether the faunistic composition of rural areas adjacent to urban areas where trade occurs inuences the choice of medicinal species commercialized and the extent of wild animals used for these purposes. This information is considered important for the development of management plans for the conservation of exploited species and their habitats. 2. Methods and materials 2.1. Study area This study was carried out in the metropolitan region of Natal City which encompasses the following municipalities: Natal, Extremoz, Cear-Mirim, So Goncalo do Amarante, Macaba, Par namirim, So Jos do Mipib and Nsia Floresta (Fig. 1). Natal is the capital city of Rio Grande do Norte, a northeastern state in Brazil. The citys population is 789,896, with a total of 1,234,819 inhabitants in the surrounding metropolitan area (http://www.ibge.gov.br). Natal is located at 5 46 S, 35 12 W, in the far east of South America. The city has a total area of 170 km2 and lies on the Atlantic Ocean, at the mouth of the Potengi River. 2.2. Methods Field research was undertaken between July 2007 and February, in open fairs of the metropolitan region of Natal City, where medicinal animals products are traded. Within the metropolitan area of Natal, the open fairs that take place are: Carrasco, Santa Catarina, Rocas, Cidade da Esperanca, Nova Natal, Panorama, Santarm, Lagoa Seca, Alecrim, Parque dos Coqueiros, Macaba, Cear-Mirim, Igap, Amarante, Parnamirim, So Goncalo do Amarante, Nsia Floresta, So Jos do Mipibu and Extremoz. The sale of medicinal animal products is often associated with that of medicinal plants, and is only conducted by merchants of natural medicinal products. All 19 open fairs were visited and the merchants of natural medicine were spoken to. In 13 of these open fairs, a trade in medicinal products derived from animals was discovered and further research was therefore conducted in these areas. Information was gathered from interviews held with 24 merchants (11 women and 13 men). The data were collected through a combination of semi-structured and open-ended interviews (Huntington, 2000). While this may be a small sample size, it must be recognized that these merchants are key informants and represent the 100% of medicinal animals traders in this area. Merchants were asked to provide the vernacular name, folk use, parts used, and the mode of preparation and administration of the remedies made from each type of animal they sold. Prior informed consent was obtained for all interviews conducted. Vernacular names of species were recorded as quoted during the interviews. Zoological material was identied with the aid of specialists, through examination of voucher specimens donated by the interviewees or purchased at trading sites, and through photographs of the animal species, or their parts, taken during interviews. Whenever necessary, these procedures were supplemented by checking vernacular names provided by merchants against the scientic names, with the aid of taxonomists familiar with the study areas. Voucher specimens and/or photographs were deposited at the Department of Systematics and Ecology, Universidade Federal da Paraba. Scientic names were updated in accordance with the Integrated Taxonomic Information Systems Catalogue of Life: 2008 Annual Checklist (ITIS, 2008). The conservation status of ani-

mal species are provided according to the International Union for Conservation of Nature (IUCN, 2009), Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES, 2008), Brazils ofcial list of endangered species (MMA, 2008), and the national list of species of aquatic invertebrates and shes endangered, overexploited, or threatened by exploitation (MMA, 2004). 2.3. Data analysis The diseases treated with zootherapeutic resources quoted by the interviewees were distributed in 14 categories (Table 1), based on the classication used by the Centro Brasileiro de Classicaco de Doencas (1993) (Brazilian Center for the Classication of Dis eases). To estimate the level of agreement between interviewees over which animals to use for each category, we calculated the informant consensus factor (ICF), adapted from Heinrich et al. (1998) that looks at the variability of animals used for each treatment, and therefore the consensus between practitioners. This factor estimates the relationship between the number of use-reports in each category (nur) minus the number of taxa used (nt) and the number of use-reports in each category minus 1. ICF is thus calculated using the following formula: ICF = nur nt nur 1

The product of this factor ranges from 0 to 1. A high value (close to 1) indicates a high consensus whereby relatively few taxa (usually species) are used by a large proportion of people, while a low value indicates that the informants disagree on the taxa to be used for treating a particular illness. The relative importance (RI) of the species cited was also calculated (adapted from Bennett and Prance, 2000). Relative importance was calculated according to the following formula: RI = NCS + NP, where NCS (number of body systems) is the number of body systems treated by a given species (NCSS) divided by the total number of body systems treated by the most versatile species (NSCSV). The number of properties (NP) is obtained from the relationship between the number of properties attributed to a species (NPS) divided by the total number of properties attributed to the most versatile species (NPSV). A value of 2, is the highest possible value, indicating the most versatile species; that with the greatest number of medicinal properties. 3. Results and discussion Zootherapeutic products from a total of 23 different species belonging to 20 families and 22 genera were traded in the localities visited (Table 2 ). These include 6 species of mammal (26%), 5 species of reptile (22%), and 4 species of insect (17%). The species most frequently quoted were: Tupinambis merianaetegu (n = 20), Cerdocyon thouscrab-eating fox (n = 20), Apis melliferawestern honey bee (n = 10), Ovis ariessheep (n = 10), Melipona subnitidaa species of stingless bee (n = 9) and Caiman latirostrisbroadsnouted caiman (n = 8). All cited medicinal species have been recorded in previous studies in Brazil (Freire, 1996; Costa-Neto, 1999; Almeida and Albuquerque, 2002; Silva et al., 2004; Alves and Pereira Filho, 2007; Alves et al., 2007a,b; Confessor et al., 2009; Ferreira et al., 2009a,b,c), for example, species such as Melipona scutellaris, Apis mellifera, Caudisona durissa and Ovis aries were recorded in other studies conducted in the North and Northeast Brazil (Alves and Rosa, 2006, 2007a,b; Alves et al., 2008, 2009a,b,c,d; Ferreira et al., 2009a). The seahorse, (Hippocampus reidi), which is used to treat asthma, has previously been found to have the same properties in many other regions in Brazil (Costa-Neto, 1999; Almeida and

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56 E.S. Oliveira et al. / Journal of Ethnopharmacology 130 (2010) 5460

Fig. 1. Map of study area, municipalities of Natal, Extremoz, Cear-Mirim, So Goncalo do Amarante, Macaba, Parnamirim, So Jos do Mipib and Nsia Floresta, NE Brazil.

Albuquerque, 2002; Alves and Rosa, 2006; Silva et al., 2004; Rosa et al., 2005). Most raw materials were harvested directly from the wild, and only three domestic species were used. All of the animals found being sold occur in State of Rio Grande do Norte, with the exception of Electrophorus electricus. This nding demonstrates the importance of local biodiversity in furnishing folk medicines, in agreement with Alves and Rosa (2006) who observed that faunal composition, accessibility, and availability directly inuence the types of zootherapeutic items sold in any given region. The use of

local fauna presumably reduces the acquisition costs of zootherapy. A similar situation was described by Williams et al. (2000) in their study of the medicinal plant market in Witwatersrand, South Africa. These authors reported a greater tendency to use and sell species that could be collected by the merchants themselves in nearby biomes or from regions where the merchants had greater familiarity. These authors concluded that the use and sale of medicinal species tends to be proportional to their availability. Nevertheless, the electric-eel (Electrophorus electricus), a species that only occurs in the North of Brazil was cited by traders. Other authors

Table 1 Categories of diseases treated with zootherapic remedies in the metropolitan region of Natal City (NE Brazil), according to the International Classication of Diseases used by the World Health Organization. Categories Certain infectious and parasitic diseases Diseases of the respiratory system Diseases of the digestive system Undened illnesses Diseases and illnesses Erysipelas, worms Asthma, bronchitis, cough, inuenza, sore throat Ulcer, gastritis Inammation, cracked feet, cracked nipples, diabetes, pain in the body, hurt, weakness Swelling Arthritis, arthrosis, backache, rheumatism Wounds, wounds in childs mouth and babys head wounds Womb problems, kidney pain Hemorrhoid Furuncle, aging skin and dandruff Ear ache Hemorrhage Tumour Total of diseases 2 5 2 7 Number of species 2 17 2 8

External causes of morbidity and mortality Diseases of the musculoskeletal system and connective tissue Injuries, poisoning and other consequences of external causes Diseases of the genitourinary system Diseases of the circulatory system Diseases of the skin and subcutaneous tissue Ear (middle and inner ear) and mastoid apophysis Blood and haematopoeitic organs, and some disorders of the immune system Symptoms, signs and abnormal ndings from medical and laboratorial examination, not categorized in other part or section Mental and behavioural perturbations Total

1 4 3 2 1 3 1 1 1

3 6 5 2 1 4 3 1 3

Insomnia

1 34

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E.S. Oliveira et al. / Journal of Ethnopharmacology 130 (2010) 5460 Table 2 Animals species used in popular medicine in the open fairs in the metropolitan region of Natal City (NE Brazil). Family/species/local name Echinoderms Echinasteridae Oreaster reticulatus (Linnaeus, 1758) Starsh, Estrela-do-mar Insects Apidae Melipona scutellaris (Latreille, 1811) a Stingless bee, Abelha urucu Apidae Melipona subnitida (Ducke, 1910) a Stingless bee, Abelha jandara Number of mentions Relative importance Part used and way of administration Disease (or illness) 57

0.225

Whole animal (1)

Asthma

0.45

Honey (13)

Wounds in childs mouth and inuenza Inuenza, wounds in childs mouth, aging skin, pain in the bones sore throat, gastritis, ulcer, weakness, insomnia and hemorrhage Bronchitis, dandruff, babys head wounds and earache Inuenza, Cough and bronchitis

Honey (10, 8, 13)

Apidae Tetragonisca angustula (Latreille, 1811) a Stingless bee, Abelha mosquito Apidae Apis mellifera (Linnaeus, 1758) Africanised honey bee, Abelha italiana Reptiles Viperidae Caudisona durissa (Linnaeus, 1758) Neotropical rattlesnake, Cascavel Teiidae Tupinambis merianae (Dumril and Bibron, 1839) tegu, Tejuac Iguanidae Iguana iguana (Linnaeus, 1758) Common iguana, Camaleo Alligatoridae Caiman latirostris (Daudin, 1801) broad-snouted caiman, Jacar-do-papo-amarelo Chelidae Phrynops geoffroanus (Schweigger, 1812) Geoffroys side-necked turtle, Cgado Fishes Syngnathidae Hippocampus reidi (Linnaeus, 1758) Longsnout seahorse, Cavalo-marinho Erythrinidae Hoplias malabaricus (Bloch, 1794) Trahira, Trara Gymnotidae Electrophorus electricus (Linnaeus, 1766) Electric eel, Peixe eltrico Amphibians Ranidae Unidentied species Frog, R Leptodactylidae Unidentied species Gia Birds Rheidae Rhea americana (Linnaeus, 1758) Greater rhea, Ema Phasianidae Gallus gallus domesticus (Linnaeus, 1758) Domestic chicken, Galinha caipira Mammals Canidae Cerdocyon thous (Linnaeus, 1766) Crab-eating fox, Raposa

0.9

Honey (10)

10

0.425

Honey (10, 12, 8, 15)

0.675

Fat (1, 13)

Asthma, wounds and ulcer

20

0.775

Fat (10, 13)

Sore throat, asthma, diabetes and Earache Sore throat, tumour Wound and erysipelas Tumour and asthma

0.9

Fat (10, 4) Bones (2)

0.45

Fat (4) Skin (1, 3)

0.675

Fat (4, 10, 14)

Sore throat, ache and swelling

0.225

Whole animal (1)

Asthma

2 2

0.45 0.675

Fat (10, 5) Fat (4)

Sore throat and earache Swelling and backache

1 3

0.325 0.325

Fat (10) Whole animal (1) Fat (14)

Arthritis and arthrosis Sore throat and asthma

1 3

0.225 0.45

Fat (4) Fat (10, 13, 4)

Pain in the body Burst furuncles and asthma

20

1.45

Fat (1, 4, 13, 14, 10)

Asthma, hemorrhoid, womb problems, cracked feet, cracked nipples, worms and rheumatism Sore throat

Dasypodidae Euphractus sexcintus (Linnaeus, 1758) Sixbanded armadillo, Tatu peba Didelphidae Didelphis albiventris (Lund, 1840) Common opossum, Tacaca

0.225

Fat (10)

0.45

Meat (6)

Kidney pain and backache

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58 Table 2 (Continued./,) Family/species/local name Bovidae Ovis ries (Linnaeus, 1758) Sheep, Carneiro (capado) Number of mentions 10 Relative importance 1.225 Part used and way of administration Tallow (4) Disease (or illness) E.S. Oliveira et al. / Journal of Ethnopharmacology 130 (2010) 5460

Rheumatism, blow, Arthritis, arthrosis, to burst furuncle and crack in the feet Asthma

Cerviade Mazama sp. Veado Unidentied family Unidentied species Whale Baleia

0.225

Fat (10) Paw (1)

0.325

Fat (10, 4)

Pain in the body and inammation

(1) Tea; (2) powder, to be spread on affected area; (3) powder, to be ingested with food, (4) ointment to be rubbed in the affected area; (5) introduced in the ear; (6) ingestion of the cooked part; (7) ingestion of the crude part; (8) beverage (garrafada), obtained by mixing medicinal plants and animals; (9) mixed with alcohol and rubbed on the affected area; (10) taken as a drink; (11) concoction, taken as a drink; (12) mixed with alcoholic beverage and taken as a drink; (13) part placed on top of the affected body part; (14) taken as a coffee; (15) mixed with lemon or white green onion and taken as a drink; and (16) worn as a talisman.

also recorded the trade of Amazonian species in open fairs in the Northeast of Brazil (Alves and Rosa, 2007a; Alves et al., 2009a), indicating the existence of commercial routes for animals harvested in different biomes around the country. Rarely are whole animals used. The parts/products listed in this research included whole animal, body secretions, fat, bones, skin, meat, tallow and paw. Of these, the fat was the most cited product, being removed 15 of the 23 mentioned species. This agrees with Moura and Marques (2008), who have noted that one characteristic in common among all zootherapeutic products, whether whole animals or their parts, is their lack of use for other purposes. More than half (55%) of the medicinal products used in Remanso, Bahia, were animal by-products. Despite the widespread use of animal by-products in zootherapy in Brazil, this has not previously been quantied (Moura and Marques, 2008). These practices have also been observed by Holland in the rst half of the 20th century, whereby amulets and remedies consisting of parts of wild animals not suitable for consumption or leather, were used as a traditional form of medicine. The parts used included the horns, teeth, nails, bones, hooves, skin and fat. According to Moura and Marques (2008) this type of use is seen as a way of maximizing the provisioning potential of local resources, given that the majority of parts used as medicine are not palatable and therefore not t for consumption. In this study we found that most medicinal animal species (82.6%) are used to treat more than one ailment. This is similar to the ndings of Alves and Rosa (2007a) whose research showed that in the markets of north and northeastern Brazil, 62% of cited species for medicinal species were used to treat more than one disease. This trend is common practice in other traditional medicine systems. For example, in Mexico, the carapace and tail of the Dasypus novemcinctus (Linnaeus, 1758) are used to treat diarrhea, tuberculosis, and whooping cough, and to induce labour (Vzquez et al., 2006). In India, the fat, skin, and bile duct of the land monitor Varanus bengalensis (Daudin, 1758) are used for treating piles, rheumatism, burns, and bites from spiders and snakes (Kakati et al., 2006). In Bolivia, products derived from the Agouti paca (Linnaeus, 1766) have been documented as remedies for general body pain, leishmaniasis, snakebite, rheumatism, heart pain, pain in bones, liver pain, fever, and pain during childbirth (Apaza et al., 2003). Among the most versatile species cited during this study are Melipona subnitida and Cerdocyum thous, which are involved in the treatment of more than six diseases and ailments. On the other hand, different animal species were sometimes used to treat the same illness. For instance, products obtained from 10 different species were used to treat asthma. Folk remedies are usually prepared in one of two ways: whole animals or body parts are macerated and the resulting powder is consumed in the form of teas or it is ingested together with food;

animal secretions (urine) and fats are administered as ointments or are ingested, either pure or diluted. The interviewees in the surveyed localities indicated that zootherapeutic products are prescribed for at least 34 different illnesses. The species with the highest relative importance were: Melipona subnitida (2.0), Cerdocyum thous (1.45) and Ovis aries (1.22). A total of 146 citations of uses for medicinal animal products were cataloged (Table 3). The categories with the largest numbers of citations were: respiratory system (75 citations; 17 species), undened diseases (15 citations; 8 species), and circulatory system (14 citations; 1 species). The use of medicinal animals for respiratory disorders is also the most common category identied in other studies at other rural and urban localities in Brazil (e.g. Alves et al., 2009a,b; Alves and Rosa, 2006). The categories with the greatest ICF values were: circulatory system (1.0), respiratory system (0.78) and external causes of morbidity and mortality (0.60). The high ICF values for these categories corroborate results from other localities in northern and northeastern Brazil (Alves and Rosa, 2007a; Alves et al., 2009a). For example, in the Crato and Juazeiro do Norte markets, Cear State, the categories with the greatest ICF values were: osteomuscular system and conjunctive tissue (0.9), undened diseases (0.81), ailments caused by external agents (0.77), and respiratory system (0.76) (Ferreira et al., 2009a). Many of the same species that are used in open fairs are used in rural areas (Torres et al., 2009), and while not conclusive, this provides some evidence that these traditions are likely to have been bought to the cities through rural-urban migration of people. According to Alves and Rosa (2007a), the use of similar resources as medicines in more remote and urban areas suggest that zootherapeutic practices may function as a social conduit which, in conjunction with other factors, helps to maintain the connections between rural and peasant people living in cities and their own traditional culture and values. More specically, it indicates the potential for exchange of materials and information on illnesses and treatments between more remote and urban communities. Many of the animal species found for sale during the survey are of conservation concern. Some of the recorded species (9 out of 23) are on either the IUCN Red List of Threatened Species, CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora) list, Brazils ofcial list of endangered species (MMA, 2008), or the National List of species of aquatic invertebrates and shes endangered, overexploited or threatened by exploitation (MMA, 2004). Although the capture of these species for medicinal purposes will impact natural populations, this is likely to be small in comparison to other large-scale threats (Alves et al., 2009c,d). In the region where the research took place, human induced res and deforestation are among the main threats to biodiversity. Nonetheless the use of animals in folk medicine can represent an additional impact that together with other pressures could result in cumula-

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E.S. Oliveira et al. / Journal of Ethnopharmacology 130 (2010) 5460 Table 3 Informant consensus factor categorized by medicinal use for corporal ailment in popular medicine in the open fairs in the metropolitan region of Natal City (NE Brazil). Categories Certain infectious and parasitic diseases Diseases of the respiratory system Diseases of the digestive system Undened illnesses External causes of morbidity and mortality Diseases of the musculoskeletal system and connective tissue Injuries, poisoning and other consequences of external causes Diseases of the genitourinary system Diseases of the circulatory system Diseases of the skin and subcutaneous tissue Ear (middle and inner ear) and mastoid apophysis Blood and haematopoeitic organs, and some disorders of the immune system Symptoms, signs and abnormal ndings from medical and laboratorial examination, not categorized in other part or section Mental and behavioural perturbations Number of animal species 2 17 2 8 3 6 5 2 1 4 3 1 3 % All species 8.69 73.91 8.69 34.78 13.04 26.08 21.73 8.69 4.34 17.39 13.04 4.34 13.04 Use citation 2 75 3 15 6 10 5 2 14 5 3 1 3 % All use citations 1.37 51.37 2.05 10.27 4.11 6.85 3.42 1.37 9.58 3.42 2.05 0.68 2.05 ICF 0.00 0.78 0.50 0.50 0.60 0.44 0.00 0.00 1.00 0.25 0.00 0.00 0.00 59

8.69

1.37

0.00

tive negative effects on the populations of a number of important local species. Research on the population viability of these species is however, lacking. From a biological perspective, there is a need to increase our understanding of the biology and ecology of species commonly used as remedies to better assess the impacts of harvesting them (for medicinal or other purposes) on their wild populations. Medicinal species that are threatened should receive urgent attention, and efforts to tackle habitat loss and alteration where these animals reside could be supported by highlighting the present and future medicinal uses of such species. In this study we found that the therapeutic properties of wild animals and plants overlapped in many cases with that of domestic or cultivated species. This therefore raises the opportunity, where suitable, of replacing the use of threatened species with domesticated or cultivated ones in traditional medicine recipes. While such a strategy is of interest from a conservationist perspective, in the context of reducing the pressure on overexploited populations or legally protected species (Alves and Rosa, 2007a), the value of wild species as sources of known, and yet to be discovered medicines, remains and can potentially support the conservation of natural bio-diverse habitats. Therefore, an understanding of the cultural, and social importance of these animals is fundamental for establishing management plans directed towards the sustainable use of species, as well as wider conservation efforts to tackle large-scale threats to habitats. 4. Conclusions Twenty-three medicinal animals were sold in the surveyed markets and products extracted from them are used to treat 34 ailments. The local population therefore holds a great deal of ethnomedical knowledge that relates to their local animal resources. The widespread use of traditional zootherapy in urban areas shown in this and other studies indicates a maintained interest in these practices, despite the likely increase in accessibility of contemporary medicine. There is a high level of informant consensus in the use of specic remedies to treat problems of the circulatory system, respiratory system as well as external causes of morbidity and mortality, which demonstrates the validity of this form of folk medicine. The traditional use of natural resources may indicate the presence of biologically active components, as historic and maintained use of naturally occurring compounds often has a scientic underpinning. This and other studies on traditional medicinal uses can represent a shortcut to modern drug discovery through providing a short list of potential sources and preventing the need for com-

prehensive surveys and screening of all available ora and fauna of an area. This study therefore highlights the need for clinical investigations of the traditional remedies cited to screen for the presence of any bioactive compounds. While the impact of these practices on animal populations is unknown, the high extractive value of these animal populations and the associated knowledge for both local populations as well as pharmaceutical research needs to be considered in any conservation strategy aimed at the faunistic resources of this area.

References
Almeida, C.F.C.B.R., Albuquerque, U.P., 2002. Uso de plantas e animais medicinais no estado de Pernambuco (Nordeste do Brasil): Um estudo de caso. Interciencia 27 (6), 276284. Albuquerque, U.P., Monteiro, J.M., Ramos, M.A., Amorim, E.L.C., 2007. Medicinal and magic plants from a public market in Northeastern Brazil. Journal of Ethnopharmacology 110, 7691. Alves, R.R.N., 2009. Fauna used in popular medicine in Northeast Brazil. Journal of Ethnobiology and Ethnomedicine 5, 1. Alves, R.R.N., Rosa, I.L., 2006. From Cnidarians to mammals: the use of animals as remedies in shing communities in NE Brazil. Journal of Ethnopharmacology 107, 259276. Alves, R.R.N., Rosa, I.L., 2007a. Zootherapy goes to town: the use of animal-based remedies in urban areas of NE and N Brazil. Journal of Ethnopharmacology 113, 541555. Alves, R.R.N., Rosa, I.L., 2007b. Zootherapeutic practices among shing communities in North and Northeast Brazil: A comparison. Journal of Ethnopharmacology 111, 82103. Alves, R.R.N., Santana,G.G., 2008. Use and commercialization of Podocnemis expansa (Schweiger1812) (Testudines: Podocnemididae) for medicinal purposes in two communities in North of Brazil 4 (3), 16. Alves, R.R.N., Pereira Filho, G.A., 2007. Commercialization and use of snakes in North and Northeastern Brazil: implications for conservation and management. Biodiversity and Conservation 16, 969985. Alves, R.R.N., Rosa, I.L., Santana, G.G., 2007a. The role of animal-derived remedies as complementary medicine in Brazil. BioScience 57, 949955. Alves, R.R.N., Pereira Filho, G.A., Lima, Y.C.C., 2007b. Snakes used in ethnomedicine in Northeast Brazil. Environment, Development and Sustainability 9, 455464. Alves, R.R.N., Lima, N.H., Tavares, M.C., Souto, W.M.S., Barboza, R.R.D., Vasconcellos, A., 2008. Animal-based remedies as complementary medicines in Santa Cruz do Capibaribe, Brazil. BMC Complementary and Alternative Medicine 8, 44. Alves, R.R.N., Lo Neto, N.A., Brooks, S.E., Albuquerque, U.P.A., 2009a. Commercialization of animal-derived remedies as complementary medicine in the semi-arid region of Northeastern Brazil. Journal of Ethnopharmacology 124 (3), 600 608. Alves, R.R.N., Oliveira, M.G.G., Barboza, R.R.D., Singh, R., Lopez, L.C.S., 2009b. Medicinal Animals as Therapeutic Alternative in a Semi-Arid Region of Northeastern Brazil. Research in Complementary Medicine 16, 305312. Alves, R.R.N., Barbosa, J.A.A., Santos, S.L.D.X., Souto, W.M.S., Barboza, R.R.D., 2009c. Animal-based remedies as complementary medicines in the semi-arid region of northeastern Brazil. In: Evidence-Based Complementary and Alternative Medicine., doi:10.1093/ecam/nep134. Alves, R.R.N., Leo Neto, N.A., Santana, G.G., Vieira, W.L.S., Almeida, W.O., 2009d. Reptiles used for medicinal and magic religious purposes in Brazil. Applied Herpetology 6, 257274.

Author's personal copy

60 E.S. Oliveira et al. / Journal of Ethnopharmacology 130 (2010) 5460 Freire, F.C., 1996. Rpteis utilizados na medicina popular no Estado de Alagoas. UFAL, Macei. Heinrich, M., Ankli, A., Frei, B., Weimann, C., Sticher, O., 1998. Medicinal plants in Mexico: Healersconsensus and cultural importance. Social Science and Medicine 47, 18631875. Huntington, H.P., 2000. Using traditional ecological knowledge in science: methods and applications. Ecological Applications 10, 12701274. ITISIntegrated Taxonomic Information System, 2008. Catalogue of Life 2008 Annual Checklist. http://www.catalogueoife.org/annual-checklist/search.php (accessed on 11.8.2009). IUCNInternational Union for Conservation of Nature, 2009. IUCN red list of threatened species. http://www.iucnredlist.org. (accessed on 14.10.2009). Kakati, L.N., Bendang, A., Doulo, V., 2006. Indigenous knowledge of zootherapeutic use of vertebrate origin by the Ao tribe of Nagaland. Journal of Human Ecology 19 (3), 163167. Maca, J.M., Garca, E., Vidaurre, P.J., 2005. An ethnobotanical survey of medicinal plants commercialized in the markets of La Paz and El Alto, Bolivia. Journal of Ethnopharmacology 97, 337350. MMA (Ministrio do Meio Ambiente), 2004. Lista Nacional das espcies de invertebrados aquticos e peixes sobreexplotadas ou ameacadas de sobreexplotaco. Instruco normativa N(5, de 21 de maio de 2004. Dirio Ocial da Unio 102, 136142. Machado, A.B.M., Drummond, G.M., Paglia, A.P. (Eds.), 2008. Livro vermelho da fauna brasileira ameacada de extinco, 1st ed. MMA (Ministrio do Meio Ambiente), p. 1420 p, http://www.mma.gov.br/sitio/index.php?ido = conteudo.monta&idEstrutura = 179&idConteudo = 8122&idMenu = 8631 (accessed on 16.12.2009). Moura, F.B.P., Marques, J.G.W., 2008. Zooterapia popular na Chapada Diamantina: uma Medicina incidental? Cincia & Sade Coletiva 13, 2179 2188. Silva, M.L.V., Alves, A.G.C., Almeida, A.V., 2004. A zooterapia no Recife (Pernambuco): uma articulaco entre as prticas e a histria. Biotemas 17 (1), 95116. Rosa, I.L., Alves, R.R.N., Bonifacio, K.M., Mouro, J.S., Osrio, F.M., Oliveira, T.P.R., Nottingham, M.C., 2005. Fishers knowledge and seahorse conservation in Brazil. Journal of Ethnobiology and Ethnomedicine 1, 115. Torres, D.F., Oliveira, E.S., Alves, R.R.N., Vasconcellos, A., 2009. Etnobotnica e etnozoologia em unidades de conservaco: uso da biodiversidade na APA de Genipabu, Rio Grande do Norte, Brasil. Interciencia 34, 623629. Vzquez, P.E., Mndez, R.M., Guiascn, O.G.R., Pinera, E.J.N., 2006. Uso medicinal de la fauna silvestre en los Altos de Chiapas, Mxico. Interciencia 31 (7), 491 499. Williams, V.L., Balkwill, K., Witkowski, E.T.F., 2000. Unraveling the commercial market for medicinal plants and plant parts on the Witwatersrand, South Africa. Economic Botany 54 (3), 310327.

Alves, R.R.N., Oliveira, M.G.G., Barboza, R.R.D., Lopez, L.C.S., 2010a. An Ethnozoological Survey of Medicinal Animals Commercialized in the Markets of Campina Grande, NE Brazil. Human Ecology Review 17, 1117. Alves, R.R.N., Souto, W.M.S., Barboza, R.R.D., 2010b. Primates in traditional folk medicine: a world overview. Mammal Review 40, 155180. Alves, R.R.N., Barboza, R.R.D., Souto, W.M.S., 2003. A Global overview of canids used in traditional medicines. Biodiversity and Conservation 19, 15131522. Apaza, L., Godoy, R., Wilkie, D., Byron, E., Huanca, O., Leonard, W.L., Perz, E., ReyesGarca, V., Vadez, V., 2003. Markets and the use of wild animals for traditional medicine: a case study among the Tsimane Amerindians of the Bolivian rain forest. Journal of Ethnobiology 23, 4764. Balick, M.J., Kronenberg, F., Ososki, A.L., Reiff, M., Fugh-Berman, A., OConnor, B., Roble, M., Lohr, P., Atha, D., 2000. Medicinal plants used by Latino healers for womens health conditions in New York City. Economic Botany 54, 344357. Balick, M.J., Reiff, M., OConnor, B., Kronenberg, F., Lohr, P., Roble, M., Fugh-Berman, A., Johnson, K.D., 2003. Ethnomedicine in the urban environment: dominican healers in New York City. Human Organization 62, 1226. Bennett, B.C., Prance, G.T., 2000. Introduced plants in the indigenous pharmacopoeia of Northern South America. Economic Botany 54 (1), 90102. Centro Brasileiro de Classicaco de Doencas (CBCD), 1993. Classicaco Estatstica Internacional de Doencas e Problemas Relacionados Sade. Dcima Reviso, vol. I. Organizaco Mundial da Sade (OMS)/Organizaco Pan-Americana de Sade (OPAS), http://www.datasus.gov.br/cid10/webhelp/cid10.htm. CITES Convention on International Trade in Endangered Species of Wild Fauna and Flora (2008) Appendices I, II and III. http://www.cites.org/eng/resources/species.html (accessed on 11.8.2009). Confessor, M.V.A., Mendonca, L.E.T., Mourao, J.S., Alves, R.R.N., 2009. Animals to heal animals: ethnoveterinary practices in semi-arid region, Northeastern Brazil. Journal of Ethnobiology and Ethnomedicine 5, 37. Costa-Neto, E.M., 1999. Healing with animals in Feira de Santana city, Bahia, Brazil. Journal of Ethnopharmacology 65, 225230. Coutinho, H.D.M., Vasconcellos, A., Lima, M.A., Almeida-Filho, G.G., Alves, R.R.N., 2009. Termite usage associated with antibiotic therapy: enhancement of aminoglycoside antibiotic activity by natural products of Nasutitermes corniger (Motschulsky 1855). BMC Complementary and Alternative Medicine 9, 35. Ferreira, F.S., Brito, S.V., Ribeiro, S.C., Saraiva, A.A.F., Almeida, W.O., Alves, R.R.N., 2009a. Animal-based folk remedies sold in public markets in Crato and Juazeiro do Norte, Ceara, Brazil. BMC Complementary and Alternative Medicine 9, 118. Ferreira, F.S., Brito, S.V., Ribeiro, S.C., Almeida, W.O., Alves, R.R.N., 2009b. Zootherapeutics utilized by residents of the community Poco Dantas, Crato-CE, Brazil. Journal of Ethnobiology and Ethnomedicine 5, 21. Ferreira, F.S., Brito, S.V., Costa, J.G.M., Alves, R.R.N., Coutinho, H.D.M., Almeida, W.O., 2009c. Is the body fat of the lizard Tupinambis merianae effective against bacterial infections? Journal of Ethnopharmacology 126, 233237.