Trends in Medicinal Uses of Edible Wild Vertebrates in Brazil
The use of food medicines is a widespread practice worldwide. In Brazil, such use is often associated with wild animals, mostly focusing on vertebrate species. Here we assessed taxonomic and ecological trends in traditional uses of wild edible vertebrates in the country, through an extensive ethnobiological database analysis. Our results showed that at least 165 health conditions are reportedly treated by edible vertebrate species (), mostly fishes and mammals. However, reptiles stand out presenting a higher plasticity in the treatment of multiple health conditions. Considering the 20 disease categories recorded, treatment prescriptions were similar within continental (i.e., terrestrial and freshwater) and also within coastal and marine habitats, which may reflect locally related trends in occurrence and use of the medicinal fauna. The comprehension of the multiplicity and trends in the therapeutic uses of Brazilian vertebrates is of particular interest from a conservation perspective, as several threatened species were recorded.
Wildlife represents an immeasurable source of raw materials that support health systems of different human cultures that depend on nature as a source of medicines to treat and cure illnesses . Plants and animals have been used as medicinal sources since ancient times, and even today animal- and plant-based pharmacopeias continue to play an essential role in health care. Although plants and plant-derived materials make up the majority of the ingredients used in most traditional medical systems globally, whole animals, animal parts, and animal-derived products also constitute important elements of the materia medica [2–6].
The use of animal species as remedies, although representing an important component of traditional medicines (sometimes in association with plant species), has been much less studied than medicinal plants . However, the importance of nonbotanical remedies (those of animal and mineral origin) is emerging , resulting in a recent boom in publications focusing on zootherapy [8–11].
Brazil is well known for its rich social/cultural diversity, as represented by more than two hundred indigenous people and a range of local communities, which in turn have contributed to the high diversity of traditional knowledge and practices which include the use of medicinal animals. Indeed, animals have been used as a source of medicine in the country and have played a significant role in healing practices as many people have used animals as medicines or alternative or supplementary treatments [12, 13].
Hence, Brazil can be considered a model to extensive zootherapeutic studies, since the use of animals and animal-derived products is widespread among the country’s human cultures, as predicted by the zootherapeutic universality hypothesis . Furthermore, the concomitant use of wild animals for nutritional and medicinal purposes is also diffuse in several localities in the country, thus highlighting their important role as food medicine in well-established folk medical practices .
Recent research has highlighted the predominant use of vertebrates as medicinal fauna in different medical systems worldwide . As remarked by Perry , this is an expected trend, considering the frequent interactions between people and vertebrates—typically large-bodied animals, which may provide a wide range of medicinal products. This raises particular conservation concerns, as some of these taxa are overharvested for their medicinal uses and are now threatened .
In this article, we provide an assessment of the uses of wild edible vertebrate species in Brazilian Traditional Medicine. The study focused on the following questions: (1) which edible vertebrate taxa are mostly used in the Brazilian Traditional Medicine? (2) Do the conditions treated by medicinal resources vary with taxonomical group and/or animal’s habitat?
Data used in this research resulted from an extensive analysis of the ethnozoological database provided by the Laboratório de Etnozoologia, Universidade Estadual da Paraíba. The database comprises information from ethnozoological studies on faunal medicinal use performed in all Brazilian regions. Additional data was gathered through information available in reviews published by the laboratory researchers [17–19].
Data analysis comprised information on species of edible vertebrates used as medicines, their family classification, habitats, conservation status, and conditions to which animals were prescribed. We only considered those taxa that could be identified to species level, and the scientific nomenclature of the taxa recorded (fishes, amphibians, reptiles, and mammals) and/or habitats were in accordance with the following databases: Fishbase (Froese and Pauly, 2016; http://www.fishbase.org/), Amphibian Species of the World (http://research.amnh.org/herpetology/amphibia/index.php), The Reptile Database (http://www.reptile-database.org/), and Mammal Species of the World . With regard to habitat analysis, marine and estuarine species were grouped in the same category (i.e., coastal and marine); if a marine species was also reported to freshwater environments, it habitat was categorized as costal and marine/freshwater. Moreover, continental species which could inhabit both terrestrial and aquatic systems were considered as semiaquatic species.
The conservation status of the analysed species follows the International Union for the Conservation of Nature , the Convention on International Trade in Endangered Species of Wild Fauna and Flora , and the Brazilian red lists (decrees 444 and 445, Brazilian Ministry of Environment, 2014). Health conditions considered in this research were categorized by the International Statistical Classification of Diseases and Related Health Problems (ICD-10 Version: 2016; http://apps.who.int/classifications/icd10/browse/2016/en).
2.1. Data Analysis
All data were verified for normal distribution (Shapiro-Wilk’s test) and homogeneity of variance (Levene’s test) and nonparametric tests were performed when those assumptions were not met.
A Kruskal-Wallis test (followed by Dunn’s post hoc test) and an ANOVA were performed to determine whether the number of health conditions treated per species varied among vertebrate taxonomic groups or habitat types, respectively. Resemblance between health conditions treated (grouped into ICD’s categories) and taxonomic groups or animals’ habitat types were assessed based on Jaccard’s similarity index, where resulting matrices were used to perform cluster analyses. Due to low number of species recorded (), amphibians were excluded from all statistical analysis regarding taxonomic groups.
At least 204 edible vertebrate species have been used in Brazilian Traditional Medicine (see Table 1). Fishes were the most represented group ( species), followed by mammals (), reptiles (), birds (), and amphibians (). Most medicinal animals are aquatic (58.9%), mostly inhabiting freshwater (27.0% of total counts) and coastal/marine (26.5% of total counts) environments (Figure 1). Terrestrial and semiaquatic vertebrates corresponded to 38.7% and 2.5% of medicinal vertebrates recorded, respectively.
Edible medicinal vertebrates were reportedly used to treat 165 health conditions/diseases (see Table 2). A single illness could be treated by various animal species (e.g., 67 animal species were used in the treatment of asthma and 60 in the treatment of rheumatism), and although most species (particularly fishes, mammals, and birds) were used to treat only one (; 41.7%) or up to five illnesses (; 76.5%), several were prescribed for treating multiple illnesses (>5 conditions; , 23.5%), as shown in Figure 2. Reptiles were the most versatile group, as they were mostly used in the treatment of multiple conditions, with almost half of the species () being used to treat more than 10 illnesses (Figure 2). Indeed, from the 10 most expressive species in the treatment of multiple conditions (see Table 1), seven are reptiles, for instance, the “teju” and the boa snake (Salvator teguixin and Boa constrictor, resp.; health conditions prescribed, each), the Neotropical rattlesnake (Crotalus durissus; conditions), the green sea turtle (Chelonia mydas; conditions), and the common caiman (Caiman crocodilus; conditions). Moreover, the trahira fish (Hoplias malabaricus; prescriptions) and the two manatee species recorded (Trichechus inunguis and T. manatus; prescriptions, each) also stand out for being indicated to the treatment of multiple illnesses.
Each species was prescribed to treat a mean of (mean ± confidence interval) health conditions. Reptiles contributed with the highest mean number of diseases treated per species, while birds and fishes comprised the groups with the lowest means (Kruskal-Wallis test: ; ; ; Dunn’s post hoc test: ; Figure 3). Nonetheless, species showed similar number of prescriptions according to habitat type (; ).
Prescriptions of edible medicinal vertebrates were generalised in 20 disease categories, according to ICD-10. From those, “symptoms, signs, and abnormal clinical and laboratory findings” were the most recorded category in terms of therapeutic quotes recorded, followed by “infectious and parasitic diseases” and “injuries, poisoning, and other consequences of external causes” (Table 2).
With regard to the number of species associated with ICD-10 categories, most animals were prescribed for treating problems associated with the “musculoskeletal system and connective tissue” and the “respiratory system” (each: species; 39.2%), “injuries, poisoning, and other consequences of external causes” (67 species, 32.8%), and “symptoms, signs, and abnormal clinical and laboratory findings” (58 species, 28.4%) (Table 2).
Despite most medicinal vertebrates provide raw materials for remedies, medicinal products often have magical-religious purposes, particularly for the prevention of diseases of spiritual cause (e.g., evil eye); they were also used as amulets to prevent diseases (e.g., amulet used as a protection against snake bite). It is worth noting that many animals involved in poisoning accidents, such as stingrays and snakes, are also used in folk medicine, particularly to treat injuries caused by themselves (see Table 1).
Fishes and birds appear to have most similar use according to ICD-10 categories (Jaccard index: 94.4), as well as reptiles and mammals (Jaccard index: 90.0), resulting in two distinct clusters (Figure 4(a)). When considering resemblance between the disease categories recorded and animals’ habitat types, two distinct clusters were also formed (terrestrial, freshwater, coastal, and marine; costal and marine/freshwater and semiaquatic) (Figure 4(b)), thus reflecting highest similarities between continental habitats (terrestrial and freshwater; Jaccard index: 90.0).
With regard to species conservation status, 160 animals figure in at least one of the three red lists assessed (see Table 1). In the ICUN red list, 33 species (mainly fishes and mammals) are classified into threatened categories, mostly as vulnerable (VU; ) ones. Endangered (EN) and critically endangered (CR) species comprised six fishes and reptiles, namely, Narcine bancroftii and Pristis pectinata (CR) and Sphyrna lewini, S. mokarran, Chelonia mydas, and Eretmochelys imbricata (EN). In Brazilian red lists, most threatened animals are also considered VU (); EN species () comprise mainly fishes and mammals; and CR ones () comprise mainly fishes and marine reptiles. In CITES, 58 species are listed, especially in its Appendix II (), mammals and reptiles being the most expressive groups.
The high number of vertebrates used as medicine is not surprising given the important role played by wildlife as a source of medicines in different traditional medicine systems [8, 10, 23, 24]. The predominance of fishes and mammals in the Brazilian Traditional Medicine confirms our expectations, given that those groups comprise major targets in Brazil [25–28]. Although these two taxa have been primarily harvested for alimentary purposes, they generate a series of the inedible parts [such as bone, skin, tail, feather, liver, and bile (“fel”)], rattle (from rattlesnakes), spine, scale, penis, carapace, beak, teeth, head, nails, and horn that can be used in popular medicines. According to Moura and Marques  the use of leftover/secondary products derived from the fauna seems to be one of the most conspicuous features on the Brazilian popular zootherapy.
Zootherapeutic products, however, do not include inedible parts solely: flesh, eggs, and viscera are among some animal products used for both medicinal and alimentary purposes [1, 12, 13, 30, 31]. This corroborates the assumption that the consumption of wild vertebrates meat is often related to the purported medicinal or cultural benefits derived from the animal parts [32–35]. In a recent review study, Alves et al.  pointed out that at least 354 wild animal species are used in Brazilian Traditional Medicine, of which 157 are also used as food, evidencing that a close connection between eating and healing is common in Brazilian zootherapy. This is in line with several studies in ethnobiology and ethnopharmacology that have observed how difficult the clear separation between medicines and foods can be [36–38] and this situation includes plants and animals, essential items for the preparation of traditional medicine.
Whether for food or medicinal purposes, the consumption of wild animals can lead to the transmission of various human diseases . Van Vliet et al.  highlighted that the consumption of bushmeat for either purpose may lead to human infection by several zoonotic pathogens. Armadillos, for example, are widely used in folk medicine and are a natural reservoir of etiological agents of several zoonotic diseases that affect humans, such as leprosy, trichinosis, coccidioidomycosis or Valley Fever, Chagas disease, and typhus . Therefore, it is essential that traditional drug therapies are submitted to an appropriate benefit/risk analysis .
It was found that several medicinal vertebrates used in the Brazilian Traditional Medicine have multiple therapeutic indications. The possibility of using various remedies for the same ailment is popular because it allows adapting to the availability of the animals. The fact that some medicinal animals are being used for the same purpose suggests that different species can share similar medicinal properties and might indicate the pharmacological effectiveness of those zootherapeutic remedies .
Multiple medicinal uses become even more evident when considering reptiles, as this group comprises one of the most important animal resources related to the medicine history  and is widely used in the most important traditional pharmacopeias worldwide . Indeed, the use in traditional medicines is the human practice that involves the highest diversity of reptile species in Brazil , some of which play important roles in traditional medicines, such as the “teju” (Tupinambis teguixin) and the boa snake (Boa constrictor), which are one of the most used medicinal animals in Brazil [42, 43]. Curiously, there is a general aversion to consuming some reptile groups, such as snakes and lizards, in the country. Nonetheless, this fact does not impair the use of these animals as medicines, as it is mainly associated with popular beliefs known as “simpatias,” which, in most of the cases, state that “a person receiving a given treatment cannot know what that he/she is taking, otherwise the effect ceases” . Hence, this fact seems to favour the high use of reptile species, despite widespread aversion to those animals.
On the other hand, despite presenting the highest diversity of medicinal species, fishes were recommended to treat a comparatively low number of health conditions. This may be related to the fact that most parts of a fish are consumed as food; thus fewer products are left to be used in medicinal practices. Similarly, when considering major hunted taxa in Brazil, that is, mammals and birds [25, 26, 44], most species are also mostly consumed as food. However, the inedible parts generate “leftovers” (e.g., skin, tail, spine, scale, teeth, nails, and horn) which are among the main products used in traditional medicine. Indeed, according to Moura and Marques , the zootherapeutic use of the fauna is mainly based on derived leftovers/secondary products. Those authors also emphasise that, from the ecological theory point of view, the use of leftovers could be justified as an attempt to leverage the resources obtained from ecosystems which are inappropriate for alimentary consumption due to the mechanical difficulty of ingesting these parts, such as horns, feather, and scales. Therefore, one can expect that the diversity of leftovers provided by a species may support the potential to treat multiple diseases.
Animals from continental habitats (i.e., terrestrial and freshwater) were found to treat similar disease categories; the same could be found within coastal and marine animals. This may be related to the local distribution of the diseases treated, thus leading people to use local resources in the traditional medicine of each region. For instance, in coastal areas, the occurrence of diseases classified into the category “external causes of morbidity and mortality” is very common, due to sting/poisoning accidents caused by fishes (e.g., stingrays, catfish, and toadfish), which are often treated by zootherapeutic products derived from the animals that caused the lesions [45–48].
Natural resources play an essential role in health care in traditional medical systems, as well as in bioprospecting for new drugs [49, 50], and the interest in animal-based products has raised [49, 51, 52]. Hence, despite the available information on the chemical components and actions of some of these products, studies on fauna traditional uses still are potentially very important to shed light on several aspects of their therapeutic applications .
The comprehension of the multiplicity and trends in therapeutic uses of several vertebrate species is of particular interest from a conservation perspective, as threatened animals, such as those recorded in this and other studies  could be replaced by nonthreatened species with similar properties. However, it is important to highlight that the use of animals for both food and medicinal purposes may impose higher pressure on those species under overexploitation conditions. For instance, if the animal is solely sought for medicinal purposes, it can lead the hunter/fisher to use selective capture techniques or even release nontargeted species. On the other hand, if an animal is captured for feeding reasons and is not the main target of the hunting or fishery (e.g., due to size), it can be kept by the hunter/fisher due to some medicinal property. Hence, understanding such complex interactions and trends in the use of fauna for nutritional and medicinal purposes evidences the important role that ethnobiological and ethnopharmacological studies may play in crucial discussion on the trade-offs between animal harvesting and its sustainability towards better regulation of those practices.
Wild edible vertebrates, particularly those inhabiting aquatic environments, are used to treat a wide range of health conditions in Brazil, with reptiles consisting of the most versatile group in multiple disease prescriptions. Moreover, a trend in prescriptions was found according to animals’ habitats, as disease categories were similar within continental and within coastal and marine habitats. Several consumed species are under threat, leading to a raise in conservation concerns, particularly due to the dual function (as food and medicines) those species present.
Conflicts of Interest
The authors declare that they have no conflicts of interest.
R. R. N. Alves and I. L. Rosa, Animals in Traditional Folk Medicine: Implications for Conservation, Springer, Berlin, Germany, 2013.
F. Alakbarli, Medical Manuscripts of Azerbaijan, Heydar Aliyev Foundation, Baku, Azerbaijan, 2006.
A. Moquin-Tandon, Elements of Medical Zoology, Baillière, 1861.
J. Stephenson, Medical Zoology, And Mineralogy; Or, Illustrations and Descriptions of the Animals and Minerals Employed in Medicine, and of the Preparations Derived from Them: Including Also an Account of Animal and Mineral Poisons, John Wilson, London, UK, 1832.View at: Publisher Site
E. Unnikrishnan, Materia Medica of the Local Health Traditions of Payyannur, Centre for Development Studies, 2004.
K. P. Groark, “To warm the blood, to warm the flesh: the role of the steambath in Highland Maya (Tzeltal-Tzotzil) ethnomedicine,” Journal of Latin American Lore, vol. 20, no. 1, pp. 3–96, 1997.View at: Google Scholar
G. J. Martínez, “Use of fauna in the traditional medicine of native Toba (qom) from the Argentine Gran Chaco region: an ethnozoological and conservationist approach,” Ethnobiology and Conservation, vol. 2, no. 2, pp. 1–43, 2013.View at: Google Scholar
J. G. W. Marques, “A fauna medicinal dos índios Kuna de San Blas (Panamá) e a hipótese da universalidade zooterapica,” in Proceedings of the Anais da 46a Reunião Anual da SBPC, Vitória, Brazil, 1994.View at: Google Scholar
A. Perry, “Global survey of marine medicinals,” in Proceedings of the 1st International Workshop on the Management and Culture of Marine Species Used in Traditional Medicines, M.-A. Moreau, H. J. Hall, and A. C. J. Vincent, Eds., pp. 35–43, Project Seahorse, Montreal, Canada, 2000.View at: Google Scholar
R. R. N. Alves, G. G. Santana, and I. L. Rosa, “The role of animal-derived remedies as complementary medicine in Brazil,” in Animals in Traditional Folk Medicine: Implications for Conservation, R. R. N. Alves and I. L. Rosa, Eds., pp. 289–301, Springer, Berlin, Germany, 2013.View at: Google Scholar
D. E. Wilson and D. M. Reeder, Mammal Species of the World, a Taxonomic and Geographic Reference, The Johns Hopkins University Press, Baltimore, Md, USA, 3rd edition, 2005.
D. Ashwell and N. Walston, An Overview of the Use and Trade of Plants and Animals in Traditional Medicine Systems in Cambodia, TRAFFIC Southeast Asia, Greater Mekong Programme, Ha Noi, Vietnam, 1st edition, 2008.
V. L. Williams, A. B. Cunningham, R. K. Bruyns, and A. C. Kemp, “Birds of a feather: quantitative assessments of the diversity and levels of threat to birds used in African traditional medicine,” in Animals in Traditional Folk Medicine: Implications for Conservation, R. R. N. Alves and I. L. Rosa, Eds., pp. 383–420, Springer, 2013.View at: Google Scholar
R. S. de Melo, O. C. da Silva, A. Souto, R. R. N. Alves, and N. Schiel, “The role of mammals in local communities living in conservation areas in the Northeast of Brazil: an ethnozoological approach,” Tropical Conservation Science, vol. 7, no. 3, pp. 423–439, 2014.View at: Publisher Site | Google Scholar
M. S. P. Rocha, J. S. Mourão, W. M. S. Souto, R. R. D. Barboza, and R. R. N. Alves, “Uso dos recursos pesqueiros no Estuário do Rio Mamanguape, Estado da Paraíba, Brasil,” Interciencia, vol. 33, no. 12, pp. 903–909, 2008.View at: Google Scholar
F. B. P. Moura and J. G. W. Marques, “Zooterapia popular na Chapada Diamantina: uma Medicina incidental?” Ciência & Saúde Coletiva, vol. 13, pp. 2179–2188, 2008.View at: Google Scholar
F. S. Ferreira, S. V. Brito, W. de Oliveira Almeida, and R. R. N. Alves, “Conservation of animals traded for medicinal purposes in Brazil: can products derived from plants or domestic animals replace products of wild animals?” Regional Environmental Change, vol. 16, no. 2, pp. 543–551, 2016.View at: Publisher Site | Google Scholar
J. B. Thorbjarnarson, C. J. Lagueux, D. Bolze, M. W. Klemens, and A. B. Meylan, “Human use of turtle: a worldwide perspective,” in Turtle Conservation, M. W. Klemens, Ed., pp. 33–84, Smithsonian Institution Press, London, UK, 2000.View at: Google Scholar
E. L. Bennett and J. G. Robinson, “Hunting of wildlife in tropical forests,” The World Bank Environment Department Papers 76, 2000.View at: Google Scholar
N. L. Etkin, Eating on the Wild Side: The Pharmacologic, Ecologic and Social Implications of Using Noncultigens, University of Arizona Press, 2000.
A. Pieroni and A. Grazzini, “Alimenti-medicina di origine animale,” in Herbs, Humans and Animals/Erbe, Uomini e Bestie, A. Pieroni, Ed., pp. 155–171, VDM, London, UK, 1999.View at: Google Scholar
R. R. N. Alves, W. L. S. Vieira, G. G. Santana, K. S. Vieira, and P. F. G. P. Montenegro, “Herpetofauna used in traditional folk medicine: conservation implications,” in Animals in Traditional Folk Medicine: Implications for Conservation, R. R. N. Alves and I. L. Rosa, Eds., pp. 109–133, Springer, Berlin, Germany, 2013.View at: Publisher Site | Google Scholar
H. Fernandes-Ferreira, S. V. Mendonça, R. L. Cruz, D. M. Borges-Nojosa, and R. R. N. Alves, “Hunting of herpetofauna in montane, coastal and dryland areas of Northeastern Brazil,” Herpetological Conservation and Biology, vol. 8, no. 3, pp. 652–666, 2013.View at: Google Scholar
A. Begossi, “Food taboos at Búzios Island (SE Brazil): their significance and relation to folk medicine,” Journal of Ethnobiology, vol. 12, no. 1, pp. 117–139, 1992.View at: Google Scholar
E. N. Anderson, D. Pearsall, E. Hunn, and N. Turner, “Ethnozoology of caiçaras from Aventureiro, Ilha Grande,” Journal of Ethnobiology, vol. 21, no. 1, pp. 107–135, 2001.View at: Google Scholar
A. Begossi and M. Ramires, “Fish folk medicine of Caiçara (Atlantic Coastal forest) and Caboclo (Amazon forest) communities,” in Animals in Traditional Folk Medicine: Implications for Conservation, R. R. N. Alves and I. L. Rosa, Eds., pp. 91–108, Springer, Berlin, Germany, 2013.View at: Publisher Site | Google Scholar
R. R. N. Alves and U. P. Albuquerque, “Animals as a source of drugs: bioprospecting and biodiversity conservation,” in Animals in Traditional Folk Medicine: Implications for Conservation, R. R. N. Alves and I. L. Rosa, Eds., pp. 67–89, Springer, Berlin, Germany, 2013.View at: Google Scholar
J. Rose, C. L. Quave, and G. Islam, “The four-sided triangle of ethics in bioprospecting: pharmaceutical business, international politics, socio-environmental responsibility and the importance of local stakeholders,” Ethnobiology and Conservation, vol. 1, no. 2012, article 3, 2012.View at: Google Scholar
E. Chivian, Biodiversity: Its Importance to Human Health, Center for Health and the Global Environment, 2002.