Zootherapeutic uses of wildmeat and associated products in the semiarid region of Brazil: general aspects and challenges for conservation

Throughout the tropics, humans exploit wild animals for many purposes, including for medicinal products [1‐3]. The reasons for using such zootherapeutic products by urban or peri-urban populations are diverse [4‐7], and while for many people it is due to the lack of easy access to allopathic remedies, it is also true that the use of wild animal parts can be strongly motivated by beliefs and traditions [8‐10].

The expansion of global markets and access to modern medicine seem to have not led to a decrease in the demand for medicinal wildlife products [9, 11]. In fact, several studies have shown that urbanization and the growth of trade have actually expanded the exploitation and trafficking of wildlife [12, 13]. Additionally, the widespread exploitation of wildlife by practitioners of traditional medicine has direct implications for culture, bioprospecting, public health, and biodiversity, given the large number of species used and the growing number of taxa threatened by this type of trade [14].

Nearly 350 animal species (176 terrestrial vertebrates) are involved in the traditional Brazilian pharmacopeia [15]. However, this number is probably an underestimate in light of new research regarding zootherapy in several parts of Brazil, and the great cultural and faunal diversity of this continent-sized country [7, 16, 17]. The Northeast Region of Brazil, in particular, assuredly possesses a significant diversity of species that are hunted as sources for popular remedies and which have yet to be reported in the literature. This is because, first of all, hunting of wildlife species for medicinal purposes is a very common practice in the semiarid area of the Northeast Region of Brazil, and zootherapeutic remedies play significant roles there in the treatment of human and livestock diseases [18, 19]. Second, the semiarid area of the Northeast Region of Brazil (Caatinga phytogeographical domain) possesses a rich diversity of terrestrial vertebrates, including 511 species of birds, 156 mammals and 175 reptiles and amphibians, in parallel with cultural richness among the local human inhabitants and their diverse interactions with wildlife [20]. This scenario suggests that the region is extremely suitable for research on wildlife hunting for medicinal, as well as other, purposes.

Available knowledge concerning the use and trade of wildlife in traditional medicine has largely come from herbalists, livestock keepers, market vendors, or end consumers in urban and rural areas (e.g., [4, 19]), and not from hunters themselves. Furthermore, most of these studies took place in isolated communities (often without access to complete health services) or in public markets where medicinal products derived from animals are sold [19, 21]. Therefore, we chose to investigate the acquisition of medicinal animals by urban and peri-urban hunters in the semiarid area of the state of Paraiba in the Northeast Region of Brazil. We assumed that hunters, being users of animal-based medicines and the individuals directly involved in capturing wild specimens, would possess detailed information concerning the species considered to be sources of zootherapeutic products and the strategies for their storage and distribution.

Therefore, we sought to identify the species of wild terrestrial vertebrates used by hunters for medicinal purposes in the semiarid area of the Northeast Region of Brazil, in order to record which diseases are treated with animal-based remedies, verify the motivations for zootherapeutic animal hunting and to identify the local distribution of animal-based remedies within the market chain. Our main hypothesis is that the richness of species richness exploited by hunters for medicinal purposes is influenced by socioeconomic factors. Secondly, we hypothesize that the local use and trade of animals for medicinal purposes has, despite enforcement strategies, adapted over time into illegal exploitation supported by social networks and the expansion of technological resources.

The broad range of hunters’ ages strengthens the view that cultural as well as socioeconomic factors serve as important motivations for hunting activities [16, 49, 50]. The weak relationship between hunter age and species richness exploited, together with a lack of significant explanatory power of other socioeconomic variables in relation to species richness of medicinal bushmeat, suggest that cultural factors and hunter and end-user preferences for certain wildlife products are drivers of the trade demand and the types of bushmeat targeted by each hunter. A similar situation was observed by Baia Júnior et al. [51] in the market chain of bushmeat products in the Brazilian Amazon. The consumption of wild species as remedies in several parts of Northeast Brazil, even when alternatives are available, reveals the cultural acceptance and economic importance of this practice, especially considering the growing context of urbanization in the region. As highlighted by Ferreira et al. [6], traditional medicine is connected to cultural and biological questions regarding animal trade, but socioeconomic aspects are also essential to the maintenance of this activity. In this context, whereas traditional wildlife uses persist with adaptations in parts of the Neotropics [52], the loss of local knowledge regarding therapeutic natural resources is also remarkable [53]. This is particularly significant considering that trade in medicinal animals represents one of the available options for livelihood for a portion of local populations [7, 53].

The high prevalence of hunters involved in wildlife trade for medicinal reasons is in line with previous studies performed in tropical regions that focused on end consumers or traders (e.g., herbalists, market sellers), which showed animal-based remedies to be widely consumed wildlife products in urban and peri-urban areas, and established trade networks that deal with the storing, transporting, and selling of products in places distant from where they were originally collected [19, 54, 55]. As with hunting bushmeat for food in other tropical areas [56, 57], the illegal trade of medicinal animals in the semiarid area of the Northeast Region of Brazil provides an opportunity for immediate cash income. The predominance of local hunters engaged in the market chain of zootherapeutic products is a clear picture of how the boundary between subsistence and commercial hunting is blurred [58, 59], with personal interests and socioeconomic realities operating together to stimulate wildlife harvesting [60].

The species richness of terrestrial vertebrates recorded in the present study was higher than that reported by previous field studies in urban or peri-urban areas of the Northeast Region of Brazil (see [19, 21]). Thus, it appears that these research, which only sampled end points of the traditional medicine market chain, missed records of wild animals targeted by the medicinal value or/and of the trade of traditional medicine resources.

There is evidence that the composition, accessibility, and availability of a local fauna directly influence the taxonomic groups and products used in traditional medicine in any given region [61]. Despite the species mentioned by hunters as being native of caatinga dry forest, the importance of mammals as sources of folk remedies has also been observed in communities, villages, and urban centers in humid or semiarid regions of Neotropical countries (see [1, 6, 19]), and peri-urban or urban communities in Africa [11, 55]. Wild mammals and reptiles are likely preferred targets of hunting for medicinal purposes due to the large quantities of parts that can be acquired from them and easily used and stored (including fatty tissue, flesh, and bone) [15]. In the present study, the average of body weight (AW) of bird species was 0.56 kg, while that of reptiles was 2.26 kg and that of mammals 4.18 kg (also Table 2). In addition, in the dry forest of the Caatinga, mammals and some reptiles represent the wild fauna most encountered throughout the year, since most birds typically migrate during the dry season (see Olmos et al. [62]) and only some small-sized birds (e.g., species of Columbidae) are relatively abundant and more easily found and hunted than mammals [63].

Certain taxa seem to be hunted because of cultural preferences. For example, some of the species hunted for purposes of traditional medicine in the semiarid area of the Northeast Region of Brazil are also popular sources of animal-based remedies in other parts of Brazil and South America. Species of the family Teiidae (Salvator spp. and Tupinambis spp.), for instance, are used as ingredients in popular medicines in Argentina, Bolivia, and other regions of Brazil [19, 64, 65]. Indeed, Bonifácio et al. [66] recently suggested that Salvator merianae is the major medicinal species for semiarid areas in Brazil. The results reported by these authors reinforce previous investigations about the use of wild fauna-based remedies in areas of Caatinga in Northeast Brazil (e.g., [4, 19, 67]), and highlight the popularity of this species as a medicinal resource in this region. Local communities have historical and transgenerational knowledge of the uses of some wild species. For example, species of the family Teiidae are well-represented among Brazilian pharmacopeia [15]. The use of Salvator merianae—as well as other species of Teiidae—in popular medicines demonstrates that this animal is locally and/or ecologically important within a cultural context and on a temporal scale [66]. The popular use of a species in a traditional pharmacopeia may ultimately represent a well-constructed system of exhaustive trial and error, which leads to the selection of animals considered useful for specific treatments. These species usually represent important subjects for pharmacological studies, as has been the case for Salvator merianae [68, 69].

Although a number of authors have noted that faunal constituents of traditional medicines are often byproducts of food animals that would otherwise be discarded (see [6, 19]), we did not observe this pattern in present research. The importance of wildmeat as a zootherapeutic remedy reinforces the need for further research at the level of the hunter about use and commercialization of wildlife in traditional medicine. Intensive use of meat was clearly detected in this study because hunters are the key harvesters of this resource (see [16, 70, 71]). Other animal parts used in traditional medicines in Brazil, in particular fat of the lizards tegu and Iguana iguana and the snakes Boa constrictor and Crotalus durissus, can be easily found as therapeutics in public markets or delivered to order for use in traditional medicine [21, 72]. Studies have shown that these fats can reduce inflammatory processes [68]; however, the therapeutic role of meat has been neglected and is in need of further pharmacological investigation.

As has been reported in Brazil, and other countries where wild animal trade is fully or partially illegal [15, 54], most intermediaries of medicinal animal trade do not directly exhibit animals or animal parts for public viewing, and the ones occasionally seen for sale at markets likely represent only a tiny portion of that which is traded in a more clandestine manner. Our results also support the findings of studies [19, 21, 73] performed with final consumers and market vendors (herbalists), which found that less perishable animal parts are commonly found at these levels of the market chain because they can be processed into products more easily hidden or camouflaged in markets (e.g., bone powder, small leather pieces, animal fat in small bottles).

The notable lack of middlemen between hunters and end consumers or market vendors distinguishes local zootherapeutic trade dynamics in the semiarid area of the Northeast Region of Brazil from other bushmeat trade operations for food or medicinal purposes (e.g., [54, 74]). Based on data from field research and the literature (W.M.S.S., unpublished data [75]), we believe that middlemen are being eliminated from the local market chain by synergistic factors, which include (1) increased availability of personal transportation (especially motorcycles), which facilitates direct exchanges between hunters and their customers; (2) increased availability of mobile phones that facilitate direct contact between consumers/herbalists and hunters, even when separated by considerable distances; and (3) low commercial values of zootherapeutics compared to other wildlife products in Brazil (e.g., bushmeat, wild pets). Therefore, the illegal trade of medicinal animal parts represents a true “fast ghost market”.

The availability of zootherapeutic species is assured for hunters and the local demand despite the climatic seasonality typical of the Caatinga domain. Coupled with the use of dry parts of wild animals in traditional medicine, Ferreira et al. [6] emphasized the existence of versatile species in favoring the continued demand for zootherapeutics by satisfying consumer demands seamlessly throughout the year, with the availability and accessibility of wild animal medicines in any given season being generally assured because a number of species can be used to treat the same disease.

Although there are only a few target species that are currently threatened, this should not be taken to mean that traditional medicine has a minimal impact on populations of zootherapeutic fauna. As highlighted by others [6, 19, 76], hunting to harvest medicinal species creates additional continuous pressure on wild populations. For the White-browed Guan, Penelope jacucaca—a vulnerable cracid included in a Brazilian plan for bird conservation [77]—or for a few species of carnivores (e.g., wild Felidae and Canidae spp.), the removal of any individuals from their natural habitats creates even greater conservation concern [78, 79].

The adoption of new conservation strategies that reconcile local demand with low levels of hunting for medicinal, or other, uses is needed [80]. There is growing recognition that approaches that employ radical prohibitions only, such as the current total hunting ban in Brazil, are insufficient for curbing hunting and poaching [80, 81]. Efficient conservation policies will require adopting both biological and socioeconomic perspectives in their implementation strategies [82]. Wildlife farming, for example, offers a potential strategy for meeting local demands while minimizing the number of wild zootherapeutic animals taken in the region of the Caatinga. In order to successfully breed species used in traditional medicinal practices in captivity, it will be necessary to provide instruction to breeders and local residents of the necessity of honesty in their dealings (together with efficient local law enforcement agencies) to avoid breeding farms from acting simply as covers for introducing illegally captured wild animals into the market [83].

It is important to emphasize that wildlife farming has been established as a profitable activity in some countries [84, 85]. The monetary return from wildlife production from captive breeding systems is indeed very high for some species. For instance, investment in high-value game breeding in 2008 would have resulted 187% return on investment by the end of 2012 in South Africa [85]. Nonetheless, wildlife farming cannot be regarded as a sole strategy for wildlife conservation because of ecological, social, and economic consequences. In general, breeding production is a market-oriented activity and, thus, as a rule, only high-production species (e.g., r-strategists) or species of high profitability are incorporated into ranching strategies [85, 86]. As a consequence, non-economically important wild animals may eventually be marginalized in the process of implementing and expanding wildlife farming, resulting in intensified human-wildlife conflicts (e.g., human vs. wild carnivore conflicts). In this way, game ranching may become less compatible with broad-spectrum species conservation [87].

Based on comparative data for species targeted for breeding, Tensen [88] recognized specific criteria by which wildlife farming can benefit species conservation: (1) production cost must be less than that for wildlife black markets, (2) restocking of farms with wild specimens must not take place, (3) laundering of wildlife into legal markets must be non-existent, (4) a substantial portion of local demand for wildlife products is met by farming wild products, and (5) consumers must show a strict preferences for captive-bred specimens only. Criteria (4) and (5) in particular are key problematic points from cultural and economic perspectives. As stated by van Vliet et al. [86], the ever-increasing human population and the high demand for wild products justifies the exploration of opportunities for the production of meat and other byproducts of native species. Nonetheless, the repertoire of vertebrates known to have effective potential for captive production in South America is small, including Salvator merianae [89‐91]. The costs associated with investments into the implementation, maintenance, and marketing of wildlife farming systems are very high for small- or medium-scale producers [86]. This reality competes with what is recognized as one of the most biodiverse faunas in the world, which is by far more inexpensive and accessible for commercial and subsistence hunters [86]. The viability of a diversity of wildlife farming programs in South America is broadly dependent on governmental and/or non-governmental agencies being persistently involved in subsidizing establishment of suitable places for ranches, provisioning technical assistance, and introducing captive breeding centers to supply founder stock [89].

Although we do not have quantitative data about frequency of harvesting and consumption of species for medicinal purposes, based on the information of interviewees that hunting of the most popular species used in the local traditional medicine system is common in the surveyed areas, as well as data of other localities of North and Northeast Brazil (see [6, 21, 61]) which suggest a wide-ranging trade of wild animals for traditional medicine, it is unlikely that there is a lower level of hunting and trapping for medicinal purposes, especially for wild animals primarily harvested for meat consumption. In addition, major hunting techniques encompass dogs, firearms, and traps as described by Barboza et al. [70], Bezerra et al. [92], and Souza et al. [16]. This varied repertoire of hunting methods has been reported as efficient in the Neotropical region and associated with areas with intense faunistic exploitation [70, 93, 94].

We believe that the use of bushmeat and other wild animal products as traditional medicine is influenced in different ways by social networks. It is impossible to unlink the activities of a local community from urban reality when implementing policies are aimed at resolving problems associated with wildlife exploitation. Local preferences contribute to the construction of strategies that may enable local demand to obtain easier access to wildlife resources. There are several ways by which social networks are associated with wildlife consumption, the most popular of which is the use of wildlife products as gifts for relatives, friends, and locally important people in both rural and urban contexts (see [95, 96]). Given that zootherapeutic products are popular in both large and small cities in Northeast Brazil [6, 19] and that hunters and their relatives are also consumers of zootherapeutic remedies (this study and Policarpo et al. [7]), it is likely that such products are also interchangeable, exchanged, or even given as an item to family members, trusted people, or friends.

Removing the black trade of zootherapeutic products from market places requires some degree of trust between local clients and hunters. Hunters are unlikely to offer animals for sale to people that they do not trust or who have not been recommended by trusted people. As seen by others, especially where trade in wildlife and it byproducts is illegal and law enforcement is not negligible, the relationship between suppliers of wild animal-based remedies and their customers is defined by mutual trust and rapport [97, 98]. Thus, we also recognize that there is a well-established social relationship between suppliers of herbalists and local hunters in the surveyed areas. Social/trust networks from three perspectives (hunters—herbalists; hunters—end customers; and hunters as zootherapeutics users—other friends/relatives) enable, in a multitude of ways, the illegal distribution of wild vertebrates. This, in turn, implies that there could be considerable hidden and specialized local and regional trade in wildlife [98].

Better understanding of consumer demand and drivers of the use of medicinal animals, as already done in studies on bushmeat for food purposes [70, 86, 96], are needed for more efficient strategies for wildlife conservation. Simple top-down conservation models have proved inefficient in tropical contexts when considered as unique strategies for conservation [99]. In Brazil and other Latin American countries, despite popular knowledge about illegality of hunting and trapping, exploitation of wild species is widespread for both urban and rural contexts. As there are social groups with dependence on the use and trade of medicinal animals for subsistence purposes, as well as these products are culturally popular, conservation policies should also consider promoting the use and trade of culturally accepted and proven effective traditional medicines. Where it is indispensable for subsistence of local communities, participatory hunting management, depending on kind of target species, can still be considered as one of the multiple and concomitant strategies for the use and conservation of the wild fauna (see [56]).

This present hunter-level survey illustrated that there is still much to be learned about the dynamics of illegal wildlife trade. Zootherapy is usually neglected as a driver for hunting in the neotropical region. However, our study shows just the opposite. The hunting of wildlife for medicinal purposes is a culturally motivated activity which supplies personal demands of hunters, as well as urban users.

Additionally, hunters provided details of an undetectable scenario in previous studies on zootherapy in Brazil. In addition to a rich diversity of wild vertebrates exploited for medicinal purposes, the hunter-level data show that the hunting for medicinal purposes in the semiarid region of Brazil is mostly linked to hunting for bushmeat. Our study demystifies the idea of an illegal wildlife trade traditionally based on physical markets (e.g., street/open fairs), since the incorporation of technological resources enabled hunters to reach out to end consumers by eliminating middlemen and flourishing an even darker market. Consequently, there is a need for a reassessment of the wildlife hunting and trade scenario for the elaboration of more efficient and participative conservation strategies by Brazilian authorities.

As some of the zootherapeutic species used in Brazilian traditional medicine appear to have true pharmacological potential [68], and local residents will not desist from purchasing natural resources for their health care, the development of a legal regulatory mechanism for the acquisition and use of animals in folk medicine is urgently needed, together with studies to evaluate the pharmacological validity of zootherapeutic medicines and the risks involved in their use. Conservation research focusing on game species and identifying culturally acceptable alternatives based on plants or domestic animals are also necessary.