Our study of hunting communities in Nigeria investigates zootherapy from a zoonotic risk perspective, examining not only which animals people use for zootherapy, but how they use them (i.e., body parts used and preparation and administration practices). In addition, we analyze the sociocultural contexts of these interactions to achiever a deeper understanding of the role of zootherapy in a society which it is practiced. Our findings reveal potential zoonotic risks, generate hypotheses for epidemiological investigations of zoonotic origins, and identify possible entry points for effective reduction of human exposures to zoonoses through zootherapeutic practices.
Species encounters via zootherapy
Zootherapies included use of both wild and domestic animals, including birds, rodents, primates, bats, ungulates, carnivores, reptiles, invertebrates, elephants, and pangolins. Animal groups and species varied in their importance in zootherapies, with wild animals most important for use in traditional medicine and domestic animals among the most important species used for other cultural purposes (Smiths S ≥ 0.05; Figs. 1a and 2b). These data show that practices related to zootherapy promote human contact with high consequence groups (rodents, bats, and primates), and that within these groups nocturnal primates (potto/angwantibo) and porcupine are among the most culturally salient species used for medicine and other cultural practices, respectively.
Rodents were frequently reported as useful for zootherapy, offering potential routes for human exposures to rodent-borne zoonoses. Zootherapies included porcupine (family Hystricidae), giant pouched rats (genus Cricetomys), and flying squirrels (family Anomalure). Indeed, porcupines make up the majority of available mammal species sold as traditional medicine in markets across Africa [83] and are the preferred and most frequently hunted animals in our study region [11, 79]. Zootherapies included use of extract from raw porcupine heart soaked in liquor, consumption of porcupine intestine (which is not otherwise widely consumed due to its bitter taste [76]), and use of quills as a laceration tool (Additional File 2). Such uses of porcupine illustrate how animal parts that are raw or might otherwise be discarded, and administration practices that permeate skin barriers, could lead to transmission of zoonotic agents. The existence of similar practices in other regions of Africa suggests any associated risks may be widespread; for example, porcupine intestine is also considered medicinal in Sierra Leone, when cooked in pepper soup (per obs., J. Bonwitt), and porcupine quills are used as a tool to puncture abscess and boils in Tanzania [84]. Similarly, the zootherapeutic use of giant pouched rats (meat, intestine, and gall bladder) was reported in our study and others across Nigeria, suggesting widespread potential for exposure to zoonoses hosted by Cricetomys spp. [47, 85–88].
Porcupine and giant pouched rats are both possible reservoirs for monkeypox virus, which is currently re-emerging in Nigeria with poorly understood zoonotic origins [89–92]. However, we are unaware of the occurrence of monkeypox or other zoonoses hosted by porcupines or giant pouched rats and within our study villages. Cricetomys species and Old World porcupines have also been found to be infected with nairoviruses, the genus of bunyaviruses that includes Crimean Congo Hemorrhagic Fever [18, 93], and porcupines have been associated with anthrax outbreaks in other parts of West Africa [94]. Flying squirrels (family Anomalure) were among the most important species used for medicine. Flying squirrel fur was especially useful for treating burns (Additional File 2), again, paralleling zootherapies described in Sierra Leone [12] and suggesting extensive use of this zootherapy across West Africa. While other small rodents (e.g. mice and rats) are important household and agricultural pests throughout West Africa, they were not frequently consumed within our study communities [79], nor were they listed as useful for medicine or other cultural purposes. However, practices that might present a risk of zoonotic exposures to small rodents elsewhere include consumption of the intestine of the brush-tailed rat to ease stomach pain [12] and chewing a concoction of rodent feces wrapped in special leaves or eating of food leftover by rats to ease childbirth [95, 96]. Epidemiological investigations of rodent-borne zoonoses should therefore explicitly consider zootherapy among possible routes of zoonotic exposures.
Primates were the second most cited group for medicinal uses, and third most common for zootherapies generally (Fig. 1A). Zootherapies involving non-human primates offered points of contact with body parts that were not typically consumed, including bones, feces, hands, skin, blood, and fur. For example, the use of chimpanzee blood, bone, and meat were reported to confer strength by participants of this study (Additional File 2) and in Sierra Leone (per. obs., J. Bonwitt). Several studies have identified multiple simian retroviruses that are transmissible to humans in West and Central Africa from blood exposure [50, 97, 98]. However, examination of risk factors for primate exposure and retroviral transmission have focused on hunting, butchering, and consumption of primates [72, 99, 100]. Our data demonstrate plausible routes for exposure to simian viruses, including blood, that extend beyond the hunting and consumption of bushmeat.
Bats were used as traditional medicine in our study population, including topical application of fur to treat burns and consumption of cooked brain to enhance children’s intelligence (Additional File 2). Although bats were generally ranked as low importance for their zootherapeutic value in our study, the use of the heads of bats for zootherapy may introduce novel risks, as a diversity of lyssaviruses, rabies-like viruses with neurological tissue tropism, have been identified in bats of sub-Saharan Africa [101]. Similar reports from traditional healers in Senegal revealed frequent use of both heads and whole bodies of the Rüppel’s Horseshoe bat in potions brewed for the treatment of mental illness [102]. Other zootherapeutic uses of bats described elsewhere include the inhalation of smoke from burning bats to treat pneumonia in Tanzania [84] and consumption of bat meat to improve female fertility and celebrate religious festivals in other regions of Nigeria [47, 48]. Bats are also sold in traditional medicine markets by 49% of traders in Benin [27] and 21% of traders in South Africa for “unknown reasons” [83].
Contacts with domestic animals via zootherapy were qualitatively different from contacts with wild animals in that domestic animals were more likely to be used in cultural (vs. medicinal) practices, involved contact with live animals, such as live sacrifices, and were more likely to make use of animal blood. Although zoonoses from domestic animals are less likely to emerge than zoonoses from wildlife [103], domestic species host many zoonotic pathogens and can play important roles as intermediate hosts of wildlife-origin pathogens [19, 104] to which humans may be exposed. Future studies should also explore the use of zootherapy to cure animal diseases, given that traditional healers are also important parts of veterinary health care systems across developing countries [105], and domesticated animals can act as bridge or amplifier hosts to facilitate transmission of wildlife-origin pathogens to humans.
Other taxonomic groups used for zootherapy included pangolins, elephants, and reptiles, as well as domestic and wild birds, carnivores, and ungulates. Pangolins were used locally and were traded for unknown zootherapeutic purposes. Pangolins are also used widely for zootherapy in other regions of Nigeria [106, 107], other African countries [108, 109], and globally [110]. Recent characterization of coronaviruses similar to SARS-CoV-2 in pangolins in Asia suggests potential emerging infectious disease risks associated with pangolin trade [111]. Indeed, trade in pangolins for their medicinal properties has contributed to the near extinction of Asian pangolins, and redirected attention to African pangolins to meet demand [112], highlighting the potential zoonotic significance of human-pangolin interactions through zootherapy at multiple geographic scales.
In Nigeria, zootherapy often extends to animals not typically used for human consumption, including amphibians, skinks, shrews, small birds and rodents, and some insects [7]. However, we only identified one animal, the chameleon, used for medicine, but not otherwise consumed. While no species was considered universally taboo in our study communities, some family rules forbid consumption of certain species due to family mythologies [11]. Nevertheless, studies have shown that people will often kill, sell and/or use medicinal concoctions of animals that are undesirable or taboo to eat [7, 12, 22]. In such cases, taboos do not necessarily preclude their use among the wider community, and interactions with such species through zootherapy can remain a source of zoonotic infection. Focusing on hunting for consumption alone can therefore blind researchers to human-animal interactions and potential zoonotic exposures through zootherapy.
Our results show that human-animal interactions with species via zootherapy are not static in space and time, as use of certain animals is subject to availability of ingredients within ecological and cultural settings, and in relation to broader trade networks, and socioeconomic constraints [113]. For example, early ethnographic accounts from our study region describe uses of animals such as leopards and manatees in zootherapy in this region of Nigeria [78], however; species declines prohibit their availability for such uses in modern contexts. Indeed, we identified high plasticity in zootherapeutic practices, including several examples of zootherapies involving the replacement of rare animals with more common or domestic species (e.g., replacement of leopard parts with those from other wild and domestic cats). The use of bat fur to cure burns also appeared to be an adaptation of the more common practice of using flying squirrel fur. Species that do not have specific zootherapeutic uses at a certain place and time may have been used in the past or may act as a substitute for similar animals in the future.
Zootherapeutic practices that can modify exposure risks
Our data provide insight into zootherapeutic prescriptions, including preparation and administration practices, that may increase or decrease risk of potential exposure to zoonotic pathogens. Use of animal parts and by-products within zootherapies that would otherwise be discarded creates unique forms of interspecies interactions that may generate zoonotic exposures. For example, the use of feces, especially from primates, in many medicinal concoctions could facilitate the spread of enteric pathogens with infective stages that are shed in feces [114, 115], whereas the use of chimpanzee blood could facilitate transmission of blood-borne pathogens, such as simian retroviruses. The practice of using animal brains and skulls may generate exposure to lyssaviruses, rabies-like viruses with neurological tissue tropism [93]. In addition, therapies that make use of dried animal parts (e.g., powders or animal skins) may pose a unique risk for zoonotic pathogen exposures. Animal skins have been implicated as a source of anthrax spores in endemic countries and through trade in animal parts [116], and other pathogens such as orthopoxviruses, including monkeypox, can have substantial lengthy environmental survival in tissue [117]. Our data highlight that low-utility animal parts that do not feature prominently in diets are still handled within communities via zootherapeutic practices, creating novel exposure risks.
Exposure risks may be mitigated or exacerbated by preparation and administration practices, which are not widely reported in zootherapy research. For example, practices that heat inactivate or soak animal parts and by-products in alcohol prior to their administration may reduce exposure risks. Time and temperature needed for pathogen inactivation is significantly affected that the type of microorganism and where it is located (e.g., tissue vs. feces) [118]. Given the variation in heating techniques (e.g., boiling, smoking, sun-drying) applied to a wide diversity of animals and animal parts, we expect higher variability in exposure risks associated with handling animals for zootherapy compared to hunting and consumption. Similarly, the use of local alcohol (traditionally, distilled palm wine) to prepare zootherapies could help to inactive some pathogens. However, disinfecting properties of locally produced alcohol are unknown. A 60%-70% alcohol solution is recommended for sterilizing contaminated objects in healthcare settings [119]. Studies from Nigeria show that locally distilled palm wine ranges from 41–78% alcohol [120], though the range is likely larger due to variation in distillation methods as well as the common practice of diluting local liquor with water. Even at high alcohol levels, liquor may be ineffective in deeper tissues, and reports of substituting liquor with water would negate any possible risk reduction associated with this practice. Importantly, preparation norms that may reduce risks to end-users’ would not decrease exposure risks in individuals procuring and preparing animal products.
Zootherapy administration practices included subcutaneous, topical, inhalation, oral, and anal exposure routes that alter the way that animal products and potentially infectious pathogens can enter the body. Parenteral (non-oral) routes of administration that by-pass the skin and mucous membranes may increase infection risks beyond what which would be expected from hunting and consumption of animal products. For example, the common practice of making incisions is likely to enhance infection risks from zoonotic pathogens as well as general infection from use of non-sterile products. Inhalation routes were described for zootherapies involving ungulates and rodents, which are known to transmit anthrax and hanta- and arena viruses, respectively. Rodent-borne hantaviruses and arenaviruses can be transmitted when virus particles are aerosolized on dust particles, such that people are advised to avoid raising dust to reduce chances of breathing it in [122, 123]. Variation in administration practices could in turn affect the type and severity of disease; for example, the illness associated with anthrax varies depending on how it enters the body, with inhalation anthrax considered to be the deadliest form [121].
In our study, relatively few zootherapies included administration of live animals, fresh parts, raw meat, or blood, suggesting that risks to end-users are low relative to those who procure and prepare zootherapies. For example, the use of animal blood was reported in only a few descriptions of zootherapies (domestic animals and primates). Still, the hunting and butchering of animals during or prior to their preparation for zootherapy involves extensive contact and environmental contamination with animal blood. It was difficult to pinpoint where blood exposures related to zootherapy might occur, because animals could be obtained by either hunters, healers, or end-users, and prepared by friends, family members, designated healers, or users. Future studies examining zootherapy value chains would be better suited to determine product preparation to further assess the risk of zoonotic exposures across these groups.
Sociocultural contexts of zootherapeutic practice
Nineteen percent of participants reported using zootherapy for themselves and their family, which is similar to other regions within Sub Saharan Africa (23% in Uganda [124]). Use of zootherapies was patterned by livelihoods, with male hunters significantly more likely than male non-hunters to use animals for medicine for themselves and their family, perhaps due to ease of access to animals and enhanced knowledge of animals. Village proximity to the forest was not associated with the likelihood that individuals used zootherapies, despite observed differences in wildlife consumption between these areas [76]. Together, these data show that zootherapy is widespread in our study region, but that increased use of animal products by hunters and their families may further contribute to heightened zoonotic exposure risks associated with hunting as an occupation.
Several zootherapeutic uses of animals were specific to certain groups (i.e., men, women, and children) or seasons, which could further pattern exposure risks. For example, some administration practices (e.g., enemas) and contact with certain animals and body parts (e.g., primate feces and bat brain) were limited to zootherapies that treated children. Other animals, including non-human primates and red duiker, featured prominently in zootherapies for prenatal care. Seasonal patterns (e.g., use of animals to treat seasonal infections such as malaria, cold/catarrh, and heat stroke, or for celebration of annual festivals or holidays) may further heighten contact in certain times of the year. Such information could be used for deciphering the epidemiology of zoonotic diseases and/or targeting interventions, for example, to hunters or including messaging about zootherapies in maternal healthcare programs.
Salient practices were difficult to define within our study area due to high variability in parts used and their preparation and administration. Indeed, traditional medicinal practices can be highly variable when: people practice do-it-yourself home remedies, treatments have high failure rates, practitioners compete with one another using different curative techniques, or treatments are prescribed within transitioning healthcare systems [125]. For instance, the value of traditional remedies can lay in their strangeness, which can conceal any uncertainty and lack of knowledge and further engender secrecy. High failure rates characteristic of traditional medicine can thus paradoxically encourage, rather than prevent, proliferation and diversification of cure. Variability in zootherapeutic practices may also reflect transitioning health systems that borrow from both local and global knowledge, combining “traditional” and “conventional” practices to meet the needs of local health systems and wildlife trade networks. In all, these results contribute to a growing number of examples showing that the practice of zootherapy in Nigeria is highly variable and lacks formulated standards or universal protocols [6, 7, 87, 126].
Our focus on people who prescribe, prepare, administer, and use zootherapies within the communities that source these animals provided a level of detail that is not always achievable in other settings, for example, trade markets. Like wildlife hunting and consumption, explorations of zootherapeutic uses of wildlife have largely focused on market surveys [85, 87, 126–129], which provide tallies of the species that are used, but offer limited information on the nature of their use due to limits in knowledge to traders who act as middlemen between hunters and end-users. Additionally, market surveys can miss species that are used locally but not widely traded [130]. Still, we were unable to determine details of animal use in zootherapies when people did not know, did not care to know, or did not want to reveal details of their practices. People may also keep certain details secret when protected species are used, patients do not want to reveal stigmatizing conditions (whether medicinal or related to witchcraft) [131], or traders do not want to expose trade secrets [83, 132, 133]. Though we tried to circumvent some of these challenges by asking about community-wide uses of animals, rather than exposing individual behavior, it is important to recognize that secrecy is embedded within traditional medicine, and there are inherent limits to the knowledge that we were able to obtain. This presents a challenge to identifying salient forms of zoonotic risks and developing interventions that target these practices.
Our data revealed some principles that may guide prescriptions of zootherapies in our study region and pattern an otherwise seemingly diverse set of practices. For example, some uses were based on bioactive components of animals (e.g., bile) or physical attributes of body parts (e.g., use of bones to give strength). Evidence from other studies shows that the condition of an animal (e.g. alive or dead) is sometimes determined by the raw materials to be extracted and the type of illness that is being treated [134]. Our results show common practices associated with different animal parts; for example, wearing or preparing powders from hard parts, using fat and feces to prepare body rubs, and ceremonial consumption of cooked meat. Public health messaging targeting administration practices for different animal parts may therefore be more effective than those that focus on specific zootherapies.
We found evidence that zootherapies were informed, in part, by sympathetic healing. For example, zootherapies included the use of skin and bones from “strong” animals for giving strength and making bullet proof charms or use of birds in making aircraft charms (Additional File 2). Pottos were used to promote strength of an unborn child when used by the pregnant mother [130]. These animals are known for their toughness and strength, with hunters reporting having to pry the animals off of tree branches after killing them [135]. The use of primate feces to cure cough was justified through observations of seeing monkeys cough in the forest; in this region where primates can serve as hosts for a zoonotic lung fluke that presents clinically with a cough [136]. Sympathetic healing also shapes contact with high risk taxa in other areas; for example, the consumption of remnants of food leftover by a rat by pregnant women to ease labor [95]. Similarly, heads and whole bodies of Rüppel’s Horseshoe bat (Rhinolophus fumigatus) were used in traditional medicines for the treatment of mental illness because bats exist as a symbol of orientation, and therefore could aid patients who by the healer’s judgment lacked mental orientation [102].
Our data also provide evidence of “like cures like” theory of healing, in which a substance capable of causing an illness or injury is also capable of curing it (e.g., the use of dog saliva to cure dog bites and snake teeth to cure snake bites). Similarly, python put into local liquor was used to prevent people from turning into a python and the bile of the python could be used to create and cure poison, depending on its preparation. Thus, while individual uses of animals were highly variable, there were patterns governing the underlying logic of their use. Indeed, the diverse use of zootherapies presents a major challenge to generalizable inclusion within public health messaging and interventions. Targeting the reasons for use of animals in medicinal and cultural practices, as opposed to specific zootherapies, may therefore be a more productive entry point for public health interventions.
Study limitations
Our study used a mixed-methods approach that focused primarily on community-wide practices to capture the breadth of zootherapies used within a single region and details of their preparation and administration. In doing so, we were unable determine the frequency by which certain products were used and how widespread their use was within and between populations. Future studies focusing on prevalence and frequency of use of different species, body parts, and preparation and administration practices across different subsets of society will be important for deciphering potential risks within these populations. Although zoonotic diseases such as monkeypox, Lassa fever, ebolavirus disease, and anthrax are known to either affect eastern Nigeria and other West African tropical rainforest communities, we do not have data on the presence of these zoonoses within our specific study communities, which have limited access to formal healthcare or diagnostic centers. Animal surveillance studies are needed to designate animals in these areas as reservoirs of zoonotic disease, and to provide direct evidence on the risks associated with different animal parts and practices. However, understanding the nature and contexts of human-animal interactions is important for assessing exposure risk. This paradigm has yielded a substantial body of research and knowledge surrounding hunting and consumption practices (e.g.,[11, 12, 72, 75, 137]), but insights into less visible forms of contact (i.e. zootherapy) have remained limited. Our mixed methods study provides a framework for examining practices in the context of zoonotic risks and generates hypotheses that will help guide surveillance for and epidemiological investigations of zoonotic pathogens.