sign in sign up
<<
Home , Bushmeat

REVIEW

Ethnobiology and Conservation 2017, 6:3 (20 April 2017) doi:10.15451/ec2017-04-6.3-1-45 ISSN 2238-4782 ethnobioconservation. com Bushmeat and health: Assessing the Evidence in tropical and sub-tropical

Nathalie Van Vliet1*, Jessica Moreno2, Juanita Gómez2, Wen Zhou1, John Emmanuel Fa1, Christopher Golden3, Rômulo Romeu Nóbrega Alves4, Robert Nasi1

ABSTRACT

The importance of bushmeat as source of and medicine for peoples calls for an appropriate benefit/risk analysis in terms of human health. In this systematic review, we compiled information on the linkages between bushmeat and health, with a particular focus on the nutritional content, the zoo-therapeutic uses and the zoonotic pool of bushmeat species in tropical and sub- regions. Despite the scarcity of data on the nutritional content of most common bushmeat species, the available studies demonstrate that bushmeat is an important source of fats, micro and macro- and has a diversity of medicinal uses. However, bushmeat may have detrimental health impacts where , transportation, handling and cooking practices do not follow food safety practices. There is evidence that some bushmeat carcasses may be contaminated by toxic metals or by polycyclic aromatic hydrocarbons. Moreover, several pathogens carried by bushmeat are found to be zoonotic and potentially transmissible to through consumption or through exposure to body fluids and feces. We stress the need for more in-depth studies on the complex links between bushmeat and human health. The development of innovative handling, conservation and cooking practices, adapted to each socio-cultural context, should help reduce the negative impacts of bushmeat consumption on human health.

Keywords: Ethnozoology, systematic review, bushmeat, , , zootherapy, health

1Center for International Forestry Research. Jalan CIFOR Situ Gede, Sindang Barang, Bogor (Barat) 16115, Indonesia.

2Fundación Science International. Calle 28 No. 13a-24. Bogotá, Colombia.

3Harvard School of Public Health. 677 Huntington Ave, Boston, MA 02115, EE. UU.

4Departamento de Biologia, Universidade Estadual da Paraíba. R. Baraúnas, 351 - Universitário, Campina Grande - PB, 58429-500, Brasil. *

1 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

INTRODUCTION sorts of animal-derived and remedies are capable of producing adverse reactions There is growing evidence that points to (Alves et al. 2013b) and the consumption of the importance of as a source of animal products as food or medicine also nutrition, medicine and spiritual values in facilitates the transmission of serious and many human cultures in tropical and widespread zoonoses. Thus, it is essential subtropical areas worldwide (Scoones et al. that traditional foods and drug therapies be 1992; Nasi et al. 2008). The of wild submitted to an appropriate benefit/risk animals in particular, commonly referred to analysis. Increased research efforts in the as bushmeat, has formed a part of the staple last decade, further spurred by recent diet of forest dwelling peoples for millennia zoonotic disease epidemics (Kurpiers et al. (Elliott et al. 2002) and remains a primary 2016), have focused attention on the source of animal , micro-nutrients and potential for bushmeat to act as a reservoir fat (Wilkie et al. 2005; Nasi et al. 2011, Siren for pathogen transmission and spread into and Machoa 2008; Golden et al. 2011; Mori at-risk human populations. et al. 2015, Alves et al. 2016). Bushmeat is To date, the role of wild in the also a significant source of revenue for many provision of human nutrition and remedies forest families (Milner-Gulland et al., 2003). and the emergence of human diseases Consumers often consider bushmeat a presents something of a paradox and wholesome, safe alternative to commercially requires an assessment of its costs and produced meat on sale at grocery stores. In benefits: “is bushmeat healthy or the some regions, it is preferred to farm-raised opposite?”. However, because nutritionists, meats for its taste or based on the ethno-zoologists and epidemiologists often perception that industrial meats contain work in isolation from one another, there is chemicals and additives (van Vliet and no compiled evidence of the links between Mbazza 2011). Moreover, bushmeat also bushmeat and health that can assist policy plays a special role in the cultural and makers in setting benchmarks of what is spiritual identity of indigenous peoples (Siren currently known and further allow 2012). Cawthorn and Hoffman (2015) have researchers to better assess the importance provided an extensive review of the nexus of the . To respond to this need, we between bushmeat and livelihoods, systematically reviewed all available emphasizing the contributions of bushmeat information on: 1) the nutrient composition of to food security, nutrition and well-being. In bushmeat 2) its use in curative or preventive some communities, human ailments are medicine and 3) the zoonotic pool present in treated with products derived from animals, bushmeat species. also known as zootherapy (Alves et al. 2013a; Begossi and Braga 1992; Johns METHODOLOGY 1996; Martinez 2013). Such animal-based preparations constitute a plethora of Our review provides a posteriori medicinal solutions employed by numerous comparison of published case studies dated cultures since ancient times, and are still up to November 2016 that illustrate the links being used in different parts of the world as between bushmeat and health. We primary or complementary treatments (Alves performed a systematic search on Google and Rosa 2013). Scholar, Web of Science and CAB Direct However, it is also well established that all (Figure 1).

2 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

Figure 1. Methodology used for the systematic review process

In Google Scholar we searched using 40 meat" OR bushmeat OR "wild meat”) AND combinations of words in English, Spanish, (nutri* OR "nutritive value" OR protein* OR Portuguese and French (Table1). The search calori* OR diet* OR consum* OR zoono* OR yielded 13827 results, excluding duplicates. pathogen* OR disease* OR illness* OR In the Web of Science database, we used infectio* OR medicin* OR "medicinal the following search string, with language properties" OR therap* OR health OR limits for articles in English, Spanish, treatment* OR "traditional medicine*" OR Portuguese, and French, and retrieved 1105 "folk medicine*" OR "alternative medicine*”). additional results: (" meat" OR "wild The search strings were developed and game" OR bushmeat OR "wild meat") AND validated among the authors, which together (nutri* OR protein* OR calori* OR diet* OR constitute a group of experts on bushmeat, consum* OR zoono* OR pathogen* OR zootherapy, nutrition and health. disease* OR illness* OR infectio* OR The references were first screened by title medicin* OR therap* OR health OR and abstract according to the primary treatment* OR "traditional medicine*" OR inclusion criteria below: "folk medicine*" OR "alternative medicine*”). 1. ONLY studies for which we were In CAB Direct, we used the following able to source the full text. Sixteen studies search string to yield 122 additional results were eliminated because their PDFs could ("game meat" OR "wild game" OR "bush not be found.

3 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

Table 1. Results of the google scholar search using several key word combinations in Spanish, Portuguese, French and English

4 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

2. ONLY studies containing tropical and sub-tropical regions were also information on the topics of interest to taken into account. our research: We selected studies only if 2. ONLY studies on bushmeat species they provided primary information on one or hunted in the wild: We did not include more of the following topics: nutritional or studies that examined meat from wild toxic content of bushmeat, pathogens found species raised in domesticated in bushmeat species with potential environments. transmission to humans (“zoonotic pool” in 3. ONLY studies referring to bushmeat bushmeat species), and zoo-therapeutic species as defined by the Bushmeat uses of bushmeat. Working Group from CITES: Bushmeat is 3. Scientific merit: To ensure the defined as “meat for human consumption scientific quality of the information reported, derived from wild animals” (CITES 2000). In we only selected peer-reviewed documents addition, the CBD working group on such as scientific journal articles, book bushmeat restricts the definition to chapters, theses for an academic degree, or , birds, reptiles and amphibians books. (Nasi et al. 2008). This definition excludes 4. ONLY studies providing primary aquatic animals, insects and molluscs. As information: Studies that used secondary such, the definition of bushmeat used here data generated by other studies were not refers to mammals, birds, reptiles and included. As far as possible, we tried to amphibians consumed by humans for food search for the primary source when it was or medicinal purposes. cited in studies found through the word 4. Our focus is on bushmeat or the use of combination search. wild animals consumed for their meat, and The references that passed this first filter not on wild animals in general. As such, for were then screened by their full text and studies that reported on presence or selected using the secondary criteria below: prevalence of zoonotic diseases, we 1. ONLY case studies from tropical and selected ONLY those that referred to sub-tropical forests: We selected studies zoonosis transmitted to humans through on bushmeat in tropical and sub-tropical the handling or consumption of forests as defined by Olson et al. (2001). bushmeat. For studies on the zoo- Tropical forests are restricted to area therapeutic uses of bushmeat, we selected between the latitudes 23.5° North and 23.5° ONLY those that described the use of South of the equator, or in other words parts of the animal that are consumed for between the Tropic of Capricorn and the therapeutic purposes (meat, intestine, Tropic of Cancer. Tropical and Sub-tropical head, penis, fat, anus, bones etc.). Several forests can be split into four areas: 1) studies on the zoonotic use of animals did Neotropical region, 2) Central / not describe any consumptive use and were Afrotropical region, 3) Oriental or therefore not included. For example, studies Indomalayan/Asian region and 4) on the use of to produce creams for Australasian region. We also included the external use or objects used for witchcraft Caatinga region in Brazil as several humid were not included in this study. Papers that forest remnants are found in this ecosystem. only described a given species as being Studies conducted in other parts of the world used for medicinal purposes without but referring to species that also occur in detailing the particular animal part(s) and its

5 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

specific use were also considered ineligible. studies shows a concentration of studies in For each of the studies that passed our Africa (n=67) (Figure 3). A few studies report filter (N=112), we extracted the following on Asia and the Pacific (India, Bangladesh, information: Australia, Malaysia, Thailand, China and - For studies on the nutritional content Papua New , n=14). In Latin America or toxic contamination of bushmeat and Caribbean (n=32), studies were species: species, part of animal tested, conducted in Brazil, Peru, Ecuador, Saint (, , Potassium, Kitts, Colombia, Mexico, French Guiana and Phosphorus, Calcium, Sodium, Manganese), Venezuela. Studies on the zoonotic potential lipids, fiber, protein, ash, carbohydrates, of bushmeat species are concentrated in moisture, toxic content and , while studies - For studies on the zoo-therapeutic on the nutritional content of bushmeat uses of bushmeat species: species, part of originate mainly from South America and the animal used, preparation, target West Africa. The zoo-therapeutic uses of population, illness prevented, illness cured, bushmeat have seen greater research ethnic origin of the users. emphasis in Latin America and particularly - For studies on the zoonotic pool of Brazil compared to any other region. bushmeat species: species, part of the animal sampled, disease agent. Nutritional content and toxic The information was organized in a contamination of bushmeat structured database. Each of the studies was recorded in the database with Studies on the nutritional content of information on authors, publication date, title, bushmeat vary in terms of the variables publication type, geographic position of analyzed (vitamins, fat, moisture, study site, country. carbohydrates, , proteins, ash, fiber, metal element contaminations), in terms of RESULTS the samples used (cooked, dried, salted, fresh, and ) and part of the General description of the data: animal used (meat, muscle, , kidney) (Annex 1). Some studies did not mention the Among the 112 studies selected, 72 species used for the analysis and the describe the zoonotic pool in bushmeat sample was only categorized as bushmeat. species, 21 report on the nutritional content Several studies conducted in sub-tropical of bushmeat and 19 report on the zoo- and tropical forests of Africa analyzed the therapeutic uses of bushmeat (Figure 2). nutritional content of bushmeat. Malaisse Over the last 5 years, there has been an and Parent (1982) concluded that exponential increase in the number of from the Miombo forest form an important studies on the zoonotic potential and subsidiary food whose nutritive value places nutritional value of bushmeat species. them on the same level as or . Studies on the zoo-therapeutic use of According to the authors, wild rodents, while bushmeat have remained rather constant not included in the F.A.O. Food Balance over the last 10 years. Sheets because they are not accounted for Within the tropical and sub-tropical forests in national surveys, make a significant biome, the geographic distribution of case contribution to the quantity and quality of

6 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

Figure 2. Number of studies per topic and year published foods eaten by communities in rural areas. most of the essential amino acids and Olawale-Abulude (2007) analyzed the phospholipids, although the skin and liver nutritional content of fresh bushmeat from a also contained high levels of cholesterol. variety of species in (including Onadeko et al. (2011) analyzed the rodents, snakes, birds, and squirrels), nutritional value of frogs (Hoplobatrachus and concluded that their use as sources of occipitalis, Xenopus muelleri and Ptychadena food was to be encouraged given their pumilio) in Nigeria and concluded that the nutritional values in terms of protein and amino acid composition of frog meat can be minerals and their good digestibility. Adei compared to those of the Clarias sp. and and Forson (2008) analyzed the livers of sp. and are valuable sources of protein grass cutters and found higher for low-income consumers. Roger et al. concentrations of iron compared to the livers (2012) analyzed the nutritional value of of domestic animals present in the market in cooked bushmeat in Northern . Similarly, Oyarekua et al. (2010) with each sample representing a different analyzed the nutrient composition of the bushmeat recipe. Niyi (2014) analyzed the African rat and concluded that the limb nutritional content for the African wild muscle was the more desirable in terms of antelope, Antilocapra americana in Nigeria and nutritive value, due to its high iron, protein, concluded that the meat was a positive potassium, magnesium and zinc content. source of protein, minerals and essential Adeyeye and Jegede (2010) and Adeyeye et amino acids and had no negative health al. (2012) analyzed the amino acid profile of implications on the consumers since it had the greater and found that its low levels of anti-nutrients (compounds that muscle, liver and skin have high levels of interfere with the absorption of nutrients). A

7 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

Figure 3. Location of case studies 8 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

recent study in Congo analyzed the fatty species in the Brazilian Amazon and acid profile of blue ’s meat and concluded that bushmeat species are porcupine meat (Mananga et al. 2015) and generally low in fat content. The meat with concluded that the consumption of those two the highest concentration of proteins was species provides essential linoleic and that of capybara (24,58g/100g). The meat arachidonic fatty acids, which contribute to with highest concentration of was the plasticity of the organism, and oleic fatty that of tapir (127,34g/100g) and the meat acid which favors the development of the with the highest content in fat was that of a good cholesterol to prevent cardiovascular Six-tubercled Amazon River diseases. (Podocnemis sextuberculata, 5.56g/100g). Additional studies in Nigeria and Ghana Cordón and Salazar de Ariza (1999) analyzed the presence of toxic elements in analyzed the nutritional content of cooked bushmeat. Adei and Forson (2008) meat from five species in Mexico (Mazama examined the livers of grass cutters in americana, Pecari tayacu, Tayassu pecari, Crax sp., Ghana and concluded that livers can be a Cuniculus paca), using a different recipe for significant source of heavy metals (Cd, Hg, each species, taking into account local Pb) in the diet. Igene et al. (2015) and culinary traditions. The study concluded that Soewu et al. (2014) analyzed metal bushmeat consumption (every 15 days as contamination on fresh and dried grass observed in the studied communities) cutter (Thryonomys swinderianus) in Nigeria contributed significantly to healthy diets due and found the meat unsafe for consumption to the high values of protein and minerals given their high concentration of nickel and contained in the bushmeat species. Galvez chromium. The authors hypothesize that et al. (1999) analyzed the nutritional content these concentration levels might come from of the four most commonly consumed contaminated and due to species in Iquitos, Peru (Tayassu pecari, or smelting waste-water production, cooking Geochelone denticulata, Agouti paca and Mazama with nickel–steel alloy utensils, and eating americana) and concluded that bushmeat from nickel-pigmented dishes. Yemi et al. contained a higher value of proteins and a (2015) found a high concentration of heavy lower fat content as compared to alternative metals in Cephalophus spp. hunted in an proteins of domestic origin (beef, mutton, agricultural from Nigeria that may , etc). Siren and Machoa (2008) be caused by acute or chronic contamination analyzed the nutrient content on bushmeat of their diet and habitat. Abdul et al. (2014) in Ecuador and found that if the availability of analyzed the polycyclic aromatic wild meat and fish decreases, the most hydrocarbons (PAH) in smoked bushmeat in serious effect would be a decrease in the Ghana and found that bushmeat smoked already low intake of fat. Felix (2012) with gas produced smaller PAH values analyzed the nutritional quality of capybara compared to bushmeat smoked using meat in Brazil and found that it presented mixed with spent oil, plastics mixed with nutritional characteristics similar to those of refuse, and discarded car tires. farmed capybara, and that the meat from For Latin America, only six studies sustainably used capybara was suitable for reported on the nutritional content of commercialization based on its nutritional bushmeat. Aguiar (1996) analyzed the qualities. The study from Lemire et al. (2010) nutrient composition of several bushmeat analyzed the content of selenium in various

9 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

foods consumed by Amazonian riverside ) to stop bleeding, the anus from populations and found that paca (1,06 μg/g) Civettictis civetta (African ) to prevent and armadillo (0,52 μg/g) meat had a higher against convulsions, the intestines of concentration of selenium than chicken and Atherurus africanus (bush tailed porcupine) to beef. Trace amounts of selenium are usually cure stomach ache, the squirrel to prevent necessary for cellular function and may be convulsions in children and python fat to important to counteract mercury (Hg) toxicity. cure rheumatism. The meat from African Only one study was found from Asia and giant snail (Achatina achatina and Achatina the Pacific. Smith et al. (1993) analyzed the marginata) is used to cure whooping cough, relationship between dietary composition anemia, ulcer, asthma, hypertension, bone and the height of children in Papua New fracture and infertility in women (Agbogidi Guinea and found that the consumption of 2010). In addition, a certain number of bushmeat (together with fresh fish) had the species are used as aphrodisiacs (the penis strongest association with increased heights, of the , baboon, squirrel, and also contained the highest protein to , buffalo, mona , tree hyraz; energy ratios and high fat to energy ratios. the entire body of the tree hyrax, tortoise, parrot; the foot of the guinea fowl; the heart Zootherapeutic uses of bushmeat or tail of the cobra, the cane rat, and the puff adder) or to increase fertility in women (the Nineteen studies report on the zoo- flesh of the warthog, , python, therapeutic uses of bushmeat to either treat baboon, tortoise; the whole body of the , or prevent illnesses, and were conducted in African giant rat, cane rat, African giant snail, India, Bangladesh, Nigeria, Brazil and squirrel and giant fowl; the placenta of the Colombia (Annex 2). Different parts of the chimpanzee and mona monkey; the intestine animals were used (e.g. the entire animal, its of the cobra, puff adder and python). meat, intestines, penis, placenta, tail, anus, In India, Solavan et al. (2014) described head, bill, gizzard), and their preparation the use of Varanus salvator prepared with the with other ingredients ( or animal skeleton and mixed with 3 liters of coconut products) were used in medicinal recipes to milk, 50g of ganja leaf, administered twice a treat multiple diseases. In total, seventy-six day for 40 days to cure arthritis, and the use bushmeat species were mentioned as of the meat from Presbytis johnii cooked with having zoo-therapeutic purposes through the seeds of Piper nigrum, the stem of Zingiber their consumption. officinale, root of the Allium sativum, cow's ghee In Nigeria, Adeola et al, (1992) described and the natural honey to cure asthma in the use of 10 species by Nigerian farmers: children below 11 years old. In Assam, India, the use of the intestines of Cephalophus Hanse and Teron (2012), described the use grimmia (grey duiker) to cure stomach ache; of cooked meat from medius (flying the use of Kinixys belliana (a tortoise) to cure fox) to cure joint pain, the use of Cervulus chest pain, the use of the intestines from muntjac, (barking deer) which legs are used to Crocodilus niloticus (Nile ) to prevent cook a soup that relieves chest pain, poisoning, the legs of Phacochoerus africanus rheumatic pain and fever, and the use of (warthog) to prevent from lameness, the Vulpes sp., fox, which flesh is cooked and penis from gorilla (gorilla) to prevent eaten to relieve joint pain and fever. The Mro from poison, the head of Manis tricuspis (tree in Bangladesh cook the meat of Sus scrofa

10 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

(Eurasian wild pig) and Canis aureus (Asian flavus as an aphrodisiac (Cuesta-Rios 2007). Jackal) to relieve arthritis and rheumatism (Chowdhury et al., 2014). Zoonotic pool in bushmeat species In Brazil, fifty one species and different with potential spillover to humans parts of the animals are consumed to treat or prevent diseases (see the long list in Annex Because the study of reservoir systems 2) (Costa-Neto 2004; Alves and Filho 2006; and how infectious agents move between Alves and Rosa 2007; Alves and Santana and within them can be complex, only a few 2008; Alves et al. 2009; Ferreira et al. 2009; cases provide evidence of the transmission Alves et al. 2010; Barros et al. 2011; Ferreira of pathogens from wildlife to humans et al. 2012; Pinto et al. 2012; Barros and (Kurpiers et al. 2016). Several pathogens Azevedo, 2014). The categories of illnesses found in bushmeat species are zoonotic and most frequently mentioned were diseases of may potentially be transmitted to humans. the respiratory tract (asthma, sore throat, However, not all of them are transmitted and cough) and the musculoskeletal system through the consumption of bushmeat itself. and connective tissue. In Mexico, Morales- Many are actually transmitted to Mavíl and Villa-Cañedo (1998) report the humans through exposure to body fluids and use of from Crotalus durissus to feces during the handling and butchering of prevent cancer, the meat from Didelphis bushmeat prior to cooking. virginiana cooked in a soup or smoked to cure skin problems and anemia, the use of the Tropical and sub-tropical forest bone from the penis of Nasua narica areas in Africa consumed as aphrodisiac and the meat from Conepatus semistriatus as a remedy against A detailed description of pathogens in acne. In Colombia, the Cofnes (an bushmeat species from Africa is also indigenous group from the Putumayo region) available in Kurpiers et al. (2016). Here, we use the whole animal of Didelphis marsupialis to specifically report on the tropical and cure acne and purify blood (Camacho- subtropical forests of Africa, where a total of Martínez 2013). The Pastos (another 50 studies describe the existence of viruses, indigenous group from the Putumayo region) bacteria, protozoa and parasites in small use Cavia porcellus for a variety of illnesses species in particular, but also in including stress, cold, weakness of the brain ungulates, birds, reptiles, rodents and and headache, weakening of the uterus in (see Annex 3). Twenty-five types of parasites women and avoid excessive salivary flow were evidenced in bushmeat species from among children (Camacho-Martínez 2013). Africa. The most abundant parasites in In the Pacific region of Colombia, rural bushmeat species were Trichuris sp., populations use the fat from Caiman crocodilus Ancylostoma sp., Ascaris, Toxoplasma gondii and fuscus to cure asthma, the biliary vesicle of Strongyloides fulleborni, most frequently Cuniculus paca as an analgesic, the liver from transmitted from simians, rodents or rodents (Proechimys semispinosus, Hoplomys ungulates to humans through a fecal-oral gymnurus, Didelphys marsupialis and Metachirus route (Annex 3: Zoonotic Parasites in nudicaudatus) as a hormonal stimulant to give bushmeat species from Africa). birth, the fat from Tamandua mexicana to cure The literature available provides records arthritis, the penis and testicles from Potos for nine main types of viruses (SIV; HTLVs,

11 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

Foamy viruses, Monkey pox, Marburg , infected animals. Tripanosoma cruzi, Lassa virus, , Nipah virus and Herpes) responsible for Chagas disease, was found that can be transmitted to humans (Wolfe et in porcupine (Coendou spp.), grey four eyed al, 2004) and is hosted mainly by small opossum (Philander opossum) and nine- , apes and Chiroptera (Annex 3: banded armadillo (Dasypus novemcinctus) Zoonotic viruses present in bushmeat of (Coura et al. 2002). Echinococcus vogeli, species in Africa). Eight types of bacteria responsable for echinococcosis disease and were reported in rodents, ungulates and Calodium hepaticum, was found in paca apes (Annex 3: Zoonotic bacteria and other (Cuniculus paca) (Almeida et al. 2013; Mayor et diseases present in bushmeat of species in al. 2015). Africa). The most common bacteria are Several bacteria responsible for Escherichia coli, Salmonella spp., and gastroenteritis and enteric diseases were Campylobacter spp. found in the raw meat of peccaries and capybara (Sarkis 2002; Annex 3: Zoonotic Latin America and Caribbean bacteria in bushmeat of species in Latin America and Caribbean) with possibilities for In Latin America and Caribbean, thirteen transmission to humans through the studies describe the presence of parasites consumption of bushmeat species in rural and bacteria in 19 bushmeat species (Annex and urban areas. Brucella suis, a type of 3: Zoonotic parasites in bushmeat of species bacteria that can cause diseases in humans in Latin America and Caribbean). Toxoplasma and domestic animals of economic gondii, a ubiquitous protozoan parasite importance alike, was found in collared capable of infecting all warm-blooded peccaries from Venezuela (Lord and Lord et animals, was found in several terrestrial al. 1991). Mycobacterium leprae was found mammals (Carme et al. 2002; Thoisy et al. in the nine-banded armadillo as well as in 2003; Da Silva 2006; Truppel et al. 2010; the six-banded armadillo (Cunga-Frota et al. Hamilton et al. 2014). Toxoplasmosis has a 2012). The exact mode of transmission of wide spectrum of clinical responses following between humans and armadillos is infection, which ranges from acute fatal not known, but several studies have shown disease, congenital disease, behavioural an association between the hunting, changes and no obvious clinical signs (Innes cleaning and eating of armadillos and the 2010). Echinococcus vogeli was found in development of leprosy in human Cuniculus paca (Mayor et al. 2015), which is populations (Clark et al. 2008; Deps et al. among the most hunted species in the 2008; Truman 2008). Armadillos are widely Amazon region. The high prevalence of used in folk medicine and are a natural polycystic echinococcosis in pacas confirms reservoir of etiological agents of several that pacas are intermediate hosts. Because zoonotic diseases that affect humans such bushmeat viscera are usually used to feed as leprosy, trichinosis, coccidioidomycosis or dogs, humans might be consequentially Valley Fever, Chaga’s disease, typhus, and infected through contact with feces from pulmonary micosis (Silva et al. 2005). infected dogs. Capillaria hepatica was found in Tayassu peccary and Ateles paniscus (Pereira- Asia and the Pacific Soares et al. 2011) and can be transmitted to humans if they consume the viscera of Very little data is available regarding the

12 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

zoonotic pool of bushmeat species from Asia content of the most important bushmeat and the Pacific. Escherichia coli and Salmonella species, particularly from the tropical forests were found in (Holds et al., of Central and West Africa. Indeed, none of 2007). Madar et al. (2012) found the the nutritional studies provide data on presence of salmonella in Axis Axis in Hawai species such as , bush tailed (see Annex 2: Zoonotic bacteria and porcupine and primates, which are among parasites in bushmeat of species in Asia and the most hunted species for food in the Pacific). Four viruses were found in tropical forests of Africa (Nasi et al. 2011). bushmeat species from Asia (Nipah virus, Another striking result is the lack of standard SARS coronavirus, Ebola, A/H5N1), methodology for the analysis of the particularly in bat species from South East nutritional content of bushmeat (part of the Asia and China (see Annex 3: Zoonotic animal, state of the sample, variables viruses present in bushmeat of species in measured, units used), which makes Asia and Pacific). comparison between studies difficult. However, the majority of studies on the DISCUSSION nutritional content of bushmeat species conclude that bushmeat contributes Our findings are constrained by the type positively to overall dietary intake. These and nature of the collected information. For results are corroborated by other studies that example, we were limited by not being able have analyzed the nutritional status of to select studies that did not make an explicit bushmeat consuming populations. In link between bushmeat and outcomes of traditional societies, bushmeat provides the interest (should they not make reference to greatest amount of daily calories (Smith et the words bushmeat, game meat, or wild al. 1993), is a crucial source of meat in the different languages used for the micronutrients (Golden et al. 2011; Sarti et search). Studies on the nutritional content, al. 2015) and fat (Siren and Machoa 2008) zoo-therapeutic uses or zoonotic pool of wild and continues to play an important role in animals that did not make explicit mention of terms of dietary diversity for modern forest consumptive use were excluded from this societies (van Vliet et al. 2015). In their search to avoid collecting information on wild literature review, King and Furgal (2014) animals more broadly without consideration provided strong arguments for the of their use as bushmeat. An alternative consumption of wild meats based on their approach to find relevant studies would have high nutritional content, especially in been to conduct a species-by-species contexts where the incidence of obesity, search based on the list of harvested diabetes, cardiovascular disease and their animals for food in each of the geographical associated adverse health outcomes are regions. However, this methodology would increasing (e.g. among indigenous groups in have expanded search efforts far beyond our the Artic). On the other hand, other studies capacity. Indeed, about 301 species for also show that many tropical forest societies mammals alone, are known to be used for have been able to substitute bushmeat with food (Ripple et al. 2016). other domestic protein sources in their Despite these limitations, a striking result dietary intake (Byron (2003) in Ecuador; of this systematic review is the paucity of Vega et al., (2013) in ). available data concerning the nutritional Concerning the zoonotic pool of

13 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

bushmeat species, the collected studies and virus (Hahon and clearly suggest that bushmeat does not Kozikowski 1961). Bushmeat can also be constitute a health risk if strict hygiene and contaminated by metals if the water, cooking food safety practices with respect to the utensils, and type of fuel used are not handling, butchering and preparation of suitable for human consumption (Abdul et al. bushmeat are followed. However, given 2014; Igene et al. 2015). The means of current practices in forest regions, hunters transportation packing methods used during may face risk of transmission if injured by an bushmeat transportation are other factors animal that is still alive, or when they carry that may cause the contamination of their prey back home, or when they cut bushmeat by pathogens. Food safety risks themselves during butchering (Subramanian stemming bushmeat handling practices from 2012), facilitating the transfer of body fluids tropical and sub-tropical forest areas is (LeBreton et al. 2006). The highest risk of nonetheless comparable to deficiencies in disease transmission actually occurs during domesticated meat handling practices in the the butchering of animals, which includes same regions due to a lack of safe water, women who engage in butchering at market waste management, adequate infrastructure and in food preparation. Very few and knowledge with regards to food safety precautions are taken by bushmeat users to practices (King and Furgal 2014). avoid contact with bodily fluids (LeBreton et Concerning the zoonotic pool of al. 2006; Yang et al. 2007; Kamins et al. bushmeat species, the available literature 2014). For example, they do not typically use highlights the significant attention paid to protective measures such as gloves (Kamins viral infections linked to bushmeat handling et al. 2014). According to Calvignac-Spencer practices (particularly that of primates) et al. (2012), increased surveillance for following the recent caused by zoonotic transmission of bushmeat zoonotic diseases (HIV and Ebola). On the pathogens to humans in areas where such other hand, bacterial and parasite infections transmission is more likely will contribute to have received less attention but constitute a a better understanding and prevention of risk major cause for the deaths of millions of factors. However, other factors besides users across tropical and sub-tropical forest hunting have also facilitated the spread of areas. These common diseases deserve retroviruses (e.g , increased closer attention. Improving access to safe urbanization, travel, increased unsafe water, gloves, and modern tools for injections and transfusions) and their impact butchering and cooking could be envisaged should also be carefully monitored to reduce among the strategies to reduce such disease transmission risks (Mouinga-Ondémé and transmission. Given the likely increase in Kazanji 2013). On the consumption side, consumption of non-traditional meats in the bushmeat may represent a risk if the meat is future (Hoffman and Cawthorn 2013), issues inadequately cooked. Roasted bushmeat that would require further research include constitutes a high risk if only superficially all facets of production and processing roasted (Sidorowicz 1974). However, following the best and most culturally bushmeat is traditionally cooked for several accepted food safety practices. hours before consumption, which reduces Several studies also report that a large such risk, including the transmission of number of animal species are used for spores (Spotts Whitney et al. 2003) medicinal purposes in rural and urban areas

14 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

worldwide, particularly in African, Asian, and “Is bushmeat healthy or the opposite?” is Latin American countries. In these areas, the not a simple question. Despite the trade of wildlife-based medicinal products is importance of this question, the existing concentrated in local and traditional markets, literature appears to have approached this where various species of medicinal question in a fragmented manner. This paper and animals are commercialized (Alves et al. demonstrates the need for more in-depth 2013b). The hygiene of medicinal products studies in tropical and sub-tropical forest sold at markets is unknown, but probably regions about the complex links between varies enormously between traders and bushmeat and human health, particularly traditional healers (Mander et al. 2007). In concerning the nutritional content of Brazil, for example, Alves and Rosa (2007) bushmeat, the pathogens that may see ranked the sanitary conditions of the zoo- zoonotic transmission and the zoo- therapeutic products as poor. Alves et al. therapeutic uses of bushmeat. The results (2013b) highlights the need for further generated should help the development and assessments of the sanitary conditions of testing of innovative approaches to reduce commercialized medicinal products, as well the negative impacts of bushmeat as the need for the implementation of consumption on human health through better measures to address the sanitary aspects of food handling and conservation practices, the trade in animals and their parts for and further acknowledge the positive medicinal or nutritional purposes. nutritional and medicinal values of bushmeat Another dimension of health that was not use. Further studies should also take into addressed in this study but that requires consideration that hunting and bushmeat further consideration is the role of mental consumption are not practiced in isolation of health. Indeed, hunting and its associated culture, society, economics, environment, social and cultural forms have shown to politics or technology. A balance needs to be contribute to the mental health and cultural struck between the quantitative perspectives continuity in traditional communities of epidemiology, and the powerful qualitative (Samson Pretty 2006). Thomas (1987) used information derived from other disciplines. the term “meat hunger” to refer to the mental Bushmeat management will depend on health problems (complaints of tiredness, understanding and working with people, with loss of vital strength and depression), related any approach based too narrowly in one or to the occasional lack of meat among the other disciplines running the risk of nomadic hunter-gatherers like African failure in the long term (Cawthorn Hoffman, Pygmies and Punan (Thomas 1987). As 2015). The reviewed literature also such, bushmeat is essential for health not demonstrates the importance of only because it is a vital source of nutrients, understanding hunting and bushmeat but also because it contributes the vitality of consumption practices within the changing hunters and communities at large (Motte- environments in which they are occurring Florac et al. 1993). According to Dounias (van Vliet et al. 2015). As such, trans- and Froment (2011), mental diseases like disciplinary approaches (including stress and depression are increasingly ethnozoology, epidemiology, anthropology, observed among former forest foragers, sociology, food technology, biology and partly because sedentism has decreased ecology, etc) need to be integrated to their access to meat from the forest. recognize that the links between bushmeat

15 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

and human health arise from highly complex Aghokeng AF, Ayouba A, Mpoudi-Ngole E, Loul interactions. S, Liegeois F, Delaporte E, Peeters M (2010) Extensive survey on the prevalence and genetic diversity of SIVs in primate bushmeat ACKNOWLEDGEMENTS provides insights into risks for potential new cross-species transmissions. This work was possible thanks to the 10(3): 386-396 financial support from USAID and UKAID, Aghokeng AF, Ayouba A, Mpoudi-Ngole E, Loul through the Bushmeat Research Initiative S, Liegeois F, Delaporte E, Peeters M (2010) Extensive survey on the prevalence and from CIFOR under the CGIAR Forest, Trees genetic diversity of SIVs in primate bushmeat and Agroforestry. program. provides insights into risks for potential new cross-species transmissions. REFERENCES 10(3): 386-396 Aghokeng AF, Bailes E, Loul S, Courgnaud V, Determinants of polycyclic aromatic Mpoudi-Ngolle E, Sharp PM, Delaporte E, hydrocarbons in smoked bushmeat. Peeters M (2007) Full-length sequence analysis of SIVmus in wild populations of mustached monkeys (Cercopithecus cephus) Determination of the from Cameroon provides evidence for two co- chemical composition of bush meats found in circulating SIVmus lineages. 360(2): Nigeria. 407-418 Aguiar JPL (1996) Notas e Comunicações. Toxic (Pb, Cd, Hg) Tabela de Composição de Alimentos da and essential (Fe, Cu, Zn, Mn) metal content Amazônia. 26(1/2): 121-126 of liver tissue of some domestic and bush Ahuka-Mundeke S, Mbala-Kingebeni P, Liegeois animals in Ghana. F, Ayouba A, Lunguya-Metila O, Demba D, Bilulu G, Mbenzo-Abokome B, Inogwabini BI, Adejinmi JO, Emikpe GE (2011) Helminth Muyembe-Tamfum JJ, Delaporte E, Peeters M parasites of some wildlife in Asejire Game (2012) Identification and molecular Reserve, Nigeria characterization of new simian T cell 41(2): 214-217 lymphotropic viruses in nonhuman primates bushmeat from the Democratic Republic of Adeola MO (1992) Importance of wild animals Congo. and their parts in the culture, religious 28(6): 628-630 festivals, and traditional medicine, of Nigeria. 19(02): 125-134 Almeida F, Caldas R, Corrêa C, Rodrigues-Silva R, Siqueira N, Machado-Silva JR (2013) Co- Adeyeye EI, Jegede RO (2010) Muscle and infections of the cestode Echinococcus skin amino acid compositions of the greater vogeli and the nematode Calodium hepaticum cane rat (Thryonomys swingerianus). in the hystricomorphic Agouti paca from a forest reserve in Acre, Brazil. 1(3): 1-9 87(04): 489-493 Adeyeye EI, Olaofe O, Ogunjana KE (2012) Alves RRN, Feijó A, Barboza RRD, Souto WMS, Lipid profiles of the skin, muscle and liver of Fernandes-Ferreira H, Cordeiro-Estrela P, greater cane rat (thryonomys swingerian us): Langguth A (2016) Game mammals of the dietary implications. 53: Caatinga biome. Ethnobiology and 11749-1175 Conservation 5:1-51 Agbogidi OM (2010) Ethno-botanical survey of Alves RRN, Filho GA (2006) Commercialization the non-timber forest products in Sapele and use of snakes in North and Northeastern Local Government Area of Delta state, Brazil: implications for conservation and Nigeria. ce 4(6): 183- management. 189 16(4):143-159

16 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

Alves RRN, Léo-Neto NA, Brooks SE, Cordón K, Salazar de Ariza J (1999) Alburquerque UP (2009) Commercialization of Composición química de carnes de animales animal-derived remedies as complementary silvestres de consumo humano en la aldea medicine in the semi-arid region of Uaxactun, Peten. Northeastern Brazil. 12(1): 5 12: 600-608 Ayouba A, Akoua-Koffi C, Calvignac-Spencer S, Alves RRN, Lima MM, Fonseca C, Dos Reis R, Esteban A, Locatelli S, Li H, Li Y, Hahn B, Figueiredo PH, Costa H, Kreuser L, Nunes MC, Delaporte E, Leendertz FH, Peeters M (2013) Ribeiro AL (2016) Peak oxygen uptake during Evidence for continuing cross-species the incremental shuttle walk test in a transmission of SIVsmm to humans: predominantly female population with characterization of a new HIV-2 lineage in Chagas heart disease. rural Côte d’Ivoire. 27(15):2488-2491 52(1): 20-27 Bachand N, Ravel A, Onanga R, Arsenault J, Alves RRN, Oliveira MDGG, Barboza RRD, Gonzalez JP (2012) Public health significance Lopez LCS (2010) An ethnozoological survey of zoonotic bacterial pathogens from of medicinal animals commercialized in the bushmeat sold in urban markets of , markets of Campina Grande, NE Brazil. Central Africa. 48(3): 17(1): 11-17 785-789 Alves RRN, Oliveira TPR, Rosa IL (2013a) Wild Barros FB, de Aguiar Azevedo P (2014) animals used as food medicine in Brazil. Common opossum (Didelphis marsupialis Linnaeus, 1758): food and medicine for 2013, 1-13. people in the Amazon. Alves RRN, Rosa IL (2007) Zootherapy goes to 10(65):1-13 town: The use of animal-based remedies in Barros FB, Pereira HM, Vicente L (2011) Use urban areas of NE and N Brazil. and knowledge of the razor-billed curassow 113: 541-555 Pauxi tuberosa (spix, 1825) (galliformes, Alves RRN, Rosa IL (2013) Introduction: cracidae) by a riverine community of the Toward a Plural Approach to the Study of Oriental Amazonia, Brazil. Medicinal Animals. In: Alves RRN Rosa IL (eds) 7(1): 1-11 Animals in Traditional Folk Medicine: implications Beer BE, Bailes E, Goeken R, Dapolito G, for conservation. Springer-Verlag, Berlin Coulibaly C, Norley SG, Kurth R, Gautier JP, Heidelberg, pp. 1-9 Gautier-Hion A, Vallet D, Sharp PM, Hirsch VM Alves RRN, Rosa IL, Albuquerque UP, (1999) Simian Immunodeficiency Virus (SIV) Cunningham AB (2013b) Medicine from the from Sun-Tailed Monkeys (Cercopithecus wild: an overview of the use and trade of solatus): Evidence for Host-Dependent animal products in traditional medicines. In: Evolution of SIV within the C. lhoesti Alves RRN, Rosa IL (eds) Animals in Traditional Superspecies. 73(9): 7734- Folk Medicine: implications for conservation. 7744 Springer-Verlag, Berlin Heidelberg, pp. 25-42 Begossi A, Braga S (1992) Food taboos and Alves RRN, Santana GG (2008) Use and folk medicine among fishermen from the commercialization of Podocnemis expansa Tocantins River(Brazil). 12(1): 101- (Schweiger 1812) (Testudines: 118 Podocnemididae) for medicinal purposes in Byron EM (2003) Market integration and two communities in North of Brazil. health: the impact of markets and 4(3), 1-6 acculturation on the self-perceived morbidity, Apetrei C, Metzger MJ, Richardson D, Ling B, diet, and nutritional status of the Tsimane’ Telfer PT, Reed P, Roberston DL, Marx PA (2005) Amerindians of lowland Bolivia. Ph.D. Detection and partial characterization of Dissertation, University of Florida, Gainesville, simian immunodeficiency virus SIVsm strains USA. from bush meat samples from rural Sierra Calattini S, Betsem EBA, Froment A, Mauclère P, Leone. 79(4): 2631-2636. Tortevoye P, Schmitt C, Njouom R, Saib A, Gessain A (2007).

17 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

transmission from apes to humans, rural immunodeficiency virus lineage with a vpu Cameroon. 13(9): gene present among different cercopithecus 1314-1320 monkeys (C. mona, C. cephus, and C. Calvignac S, Adjogoua EV, Akoua-Koffi C, nictitans) from Cameroon. Hedemann C, Schubert G, Ellerbrok H, 77(23): 12523-12534 Leendertz SAJ, Pauli G, Leendertz, F (2012) Corbet S, Müller-Trutwin MC, Versmisse P, Origin of Human T-Lymphotropic Virus Type 1 Delarue S, Ayouba A, Lewis J, Brunak S, Martin in Rural Côte d’Ivoire. P, Brun-vezinet F, Simon F, Barre-sinoussi F, 18(5):830-833 Mauclere P (2000) env sequences of simian Camacho Martínez AV (2013) El uso medicinal immunodeficiency viruses from de la fauna silvestre y sus implicaciones para in Cameroon are strongly related to those of la conservación en el municipio del Valle del human immunodeficiency virus group N from Guamuez, Putumayo, Colombia. Bachelor the same geographic area. thesis, Pontificia Universidad Javeriana, Bogotá, 74(1): 529-534 Colombia. Costa Neto EM (2004) Implications and Carme B, Bissuel F, Ajzenberg D, Bouyne R, applications of folk zootherapy in the state of Aznar C, Demar M, Bichat S, Louvel D, Bahia, Northeastern Brazil. Bourbigot AM, Peneau C, Neron P (2002) 12(3): 161-174 Severe acquired toxoplasmosis in Coura JR, Junqueira AC, Fernandes O, Valente immunocompetent adult patients in French AS, Miles MA (2002) Emerging chagas disease Guiana. 40(11): in Amazonian Brazil. 18(4): 4037-4044 171-176 Cawthorn DM, Hoffman, LC (2015) The Cuesta-Ríos EY, Valencia-Mazo JD, Jiménez- bushmeat and food security nexus: a global Ortega AM (2007) Aprovechamiento de los account of the contributions, conundrums vertebrados terrestres por una comunidad and ethical collisions. humana en bosques tropicales (Tutunendo, 76, 906-925. Chocó, Colombia). Chowdhury R, Warnakula S, Kunutsor S, Crowe 26(2): 37-43 F, Ward HA, Johnson L, Franco O, Butterworth da Silva AV, Bosco SDMG, Langoni H, Bagagli E AS, Forouhi NG, Thompson SG, Khaw KT, (2006) Study of Toxoplasma infection in Mozaffarian D, Danesh J, Angelantonio E (2014) Brazilian wild mammals: Serological evidence Association of dietary, circulating, and in Dasypus novemcinctus Linnaeus, 1758 and supplement fatty acids with coronary riska Euphractus sexcinctus Wagler, 1830. systematic review and meta-analysis. 135(1): 81-83 160(6): 398-406 de Thois B, Demar M, Aznar C, Carme B (2003) Chua KB (2003) Nipah virus outbreak in Ecologic correlates of Toxoplasma gondii Malaysia. 26(3): 265- exposure in free-ranging neotropical 275 mammals. 39(2): 456- CITES (2000) Bushmeat as a trade and 459 issue. Eleventh meeting Deps PD, Alves BL, Gripp CG, Aragao RL, of the Conference of the Parties Gigiri, Kenya. Guedes B, Filho JB, Andreatta MK, Marcari RS, Doc 11.4. Available: https://ecohealth.net/wp- Prates I, Rodriguez LC (2008) Contact with content/uploads/2016/10/ECH_Author_Info-3.pdf armadillos increases the risk of leprosy in Clark BM, Murray CK, Horvath LL, Deye GA, Brazil: a case control study. Rasnake MS, Longfield RN (2008) Case-control 74: 338- study of armadillo contact and Hansen’s 342 disease. Dounias E, Froment A (2011) From foraging to 78: 962-967 farming among present-day forest hunter- Courgnaud V, Abela B, Pourrut X, Mpoudi-Ngole gatherers: consequences on diet and health. E, Loul S, Delaporte E, Peeters M (2003) 13(3): 294-304 Identification of a new simian Elliott SS, Keim NL, Stern JS, Teff K, Havel PJ

18 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

(2002) Fructose, weight gain, and the insulin bat SARS-like coronavirus that uses the resistance syndrome. ACE2 receptor. 503(7477): 535-538 76:911–922 Golden CD, Fernald LCH, Brashares JS, Etienne L, Nerrienet E, LeBreton M, Bibila GT, Rasolofoniaina BJR, Kremen C (2011) Benefits Foupouapouognigni Y, Rousset D, Nana A, Djoko of wildlife consumption to child nutrition in a CF, Tamoufe U, Aghokeng AF, Mpoudi-Ngole E, hotspot. Delaporte E, Peeters M, Wolfe ND, Ayouba A (2011) Characterization of a new simian 108:19653–19656 immunodeficiency virus strain in a naturally Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX, infected troglodytes troglodytes Cheung CL, Luo SW, Li PH, Zhang LJ, Guan YJ, chimpanzee with AIDS related symptoms. Butt KM, Wong KL, Chang KW, Lim W, Retrovirology 8(1): 4 Shortridge KF, Yuen KY, Peiris JSM, Poon LLM Felix GA (2012) Comportamento alimentar e (2003). Isolation and characterization of qualidade de carne de capivara viruses related to the SARS coronavirus from (Hydrochoerus hydrochaeris Linnaeus, 1766) animals in southern China. 302(5643): de vida livre, em áreas agrícolas. Doctoral 276-278. dissertation, Universidade Federal da Grande Haesevelde MMV, Peeters M, Jannes G, Dourados, Dourados, Brazil Janssens W, Van der groen G., Sharp PM, Ferreira FS, Albuquerque UP, Coutinho HDM, Saman E (1996) Sequence analysis of a highly Almeida WDO, Alves RRN (2012) The trade in divergent HIV-1-related lentivirus isolated medicinal animals in northeastern Brazil. from a wild captured chimpanzee. 221(2): 346-350 2012: 1-20 Hahon N, Kozikowski E (1961) Thermal Ferreira FS, Brito SV, Ribeiro SC, Almeida WO, inactivation studies with variola virus. Alves RR (2009) Zootherapeutics utilized by 81(4): 609 residents of the community Poço Dantas, Hamilton CM, Katzer F, Beierschmitt A, Soto E, Crato-CE, Brazil. Innes EA, Kelly PJ (2014) First report of 5(11):1-10 Toxoplasma gondii seroprevalence in wild- Formenty P, Boesch C, Wyers M, Steiner C, caught Caribbean African green monkeys. Donati F, Dind F, Walker F, Le Guenno B (1999) 7(1): 1-4 Ebola virus outbreak among wild Hanse R Teron R (2012) Ethnozoological chimpanzees living in a forest of Cote practices among the Karbi tribes in Karbi d'Ivoire. 179 (1): Anglong district of Assam (India). S120-S126 1: 117-120 Frota CC, Lima LN, Rocha Ada S, Suffys PN, Hayman DT, Emmerich P, Yu M, Wang LF, Suu- Rolim BN, Rodrigues LC, Barreto ML, Kendall C, Ire R, Fooks AR, Cunningham AA, Wood JL Kerr LR (2012) Mycobacterium leprae in six- (2010) Long-term survival of an urban fruit banded (Euphractus sexcinctus) and nine- bat seropositive for Ebola and Lagos bat banded armadillos (Dasypus novemcinctus) viruses. 5(8): 1-3 in Northeast Brazil. 107: 209-213. Hoffman LC, Cawthorn D (2013) Exotic protein sources to meet all needs 95(4): Gálvez H, Arbaiza T, Carcelén F, Lucas O (1999) 764-771. Valor nutritivo de las carnes de sajino (tayassu tajacu), venado colorado (mazama Holds G, Pointon A, Lorimer M, Kiermeier A, americana), majaz (agouti paca) y motelo Raven G, Sumner J (2008) Microbial profiles of (geochelone denticulata). carcasses and minced meat from kangaroos 10(1):82-86 processed in South Australia. 123(1): 88-92. Ge XY, Li JL, Yang XL, Chmura AA, Zhu G, Epstein JH, Mazet JK, Wei Zhang BH, Peng C, Igene JO, Okoro KI, Ebabhamiegbebho PA, Zhang YJ, Luo CH, Tan B, Wang N, Zhu Y, Evivie SE (2015) A study assessing some Crameri C, Zhang SY, Wang LF, Daszak P, Shi metal elements contamination levels in ZL (2013) Isolation and characterization of a grasscutter (Thryonomys swinderianus

19 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

Temminck) meat. 85(11): 3305-3312 3(5): 63 Leendertz FH, Ellerbrok H, Boesch C, Couacy- Innes EA (2010) A brief history and overview Hymann E, Mätz-Rensing K, Hakenbeck R, of Toxoplasma gondii. Bergmann C, Abaza P, Junglen S, Moebius Y, 57(1): 1-7 Vigilant L, Formenty P, Pauli G (2004a) Anthrax Jobbins SE, Sanderson CE, Alexander KA (2014) kills wild chimpanzees in a tropical rainforest. Leptospira interrogans at the human–wildlife 430: 451-452. interface in northern Botswana: a newly Leendertz FH, Yumlu S, Pauli G, Boesch C, identified public health threat. Couacy-Hymann E, Vigilant L, Junglen S, 61(2): 113-123 Schenk S, Ellerbrok H (2006) A new Bacillus Johns T (1996) The origins of human diet and anthracis found in wild chimpanzees and a medicine. University of Arizona Press, Tucson, gorilla from West and Central Africa. USA. 2(1): 1-4 Kamins AO, Rowcliffe JM, Ntiamoa-Baidu Y, Leendertz SAJ, Junglen S, Hedemann C, Goffe Cunningham AA, Wood JL, Restif O. (2015) A, Calvignac S, Boesch C, Leendertz FH (2010) Characteristics and risk perceptions of High prevalence, coinfection rate, and genetic Ghanaians potentially exposed to bat-borne diversity of retroviruses in wild red colobus zoonoses through bushmeat. 12(1): monkeys (Piliocolobus badius badius) in Tai 104-120 National Park, Cote d'Ivoire. 84(15): 7427-7436 King U, Furgal C (2014) Is hunting still healthy? Understanding the Lemire M, Fillion M, Barbosa F, Guimarães J RD, interrelationships between indigenous Mergler D (2010) Elevated levels of selenium participation in land-based practices and in the typical diet of Amazonian riverside human-environmental health. populations. 408(19): 4076-4084 11(6): 5751-5782 Leroy EM, Telfer P, Kumulungui B, Yaba P, Kurpiers LA, Schulte-Herbrüggen B, Ejotre I, Rouquet P, Roques P, González JP, Ksiakez TG, Reeder DAM (2016) Bushmeat and emerging Rollin PE, Nerrienet E (2004) A serological infectious diseases: Lessons from Africa. In: survey of Ebola virus infection in central Angelici FM (ed) Problematic wildlife: A cross African nonhuman primates. disciplinary approach, Springer, New York, pp. 190(11): 1895-1899 507-551 Leroy EM, Rouquet P, Formenty P, Souquiere S, Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Kilbourne A, Froment JM, Bermejo M, Smit S, Wong BH, Wong SS, Leung SY, Chan KH, Yuen, Karesh W, Swanepoel R, Zaki SR (2004a) KY (2005) Severe acute respiratory syndrome Multiple Ebola virus transmission events and coronavirus-like virus in Chinese horseshoe rapid decline of central African wildlife. bats. 303(5656): 387-390 102(39): Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, 14040-14045 Wang H, Crameri G, Hu Z, Zhang H, McEachern LeBreton M, Prosser AT, Tamoufe U, Sateren W, J, Field H, Daszak P, Eaton BT, Zhang S, Wang Mpoudi Ngole E, Diffo JLD, Burke DS, Wolfe ND LF (2005). Bats are natural reservoirs of (2006) Patterns of bushmeat hunting and SARS-like coronaviruses. 310(5748): perceptions of disease risk among central 676-679. African communities. 9(4): Liégeois F, Boué V, Mouacha F, Butel C, Ondo 357-363 BM, Pourrut X, Leroy E, Peeters M, Rouet F Leendertz FH, Boesch C, Ellerbrok H, Rietschel (2012) New STLV-3 strains and a divergent W, Couacy-Hymann E, Pauli G (2004) Non- SIVmus strain identified in non-human invasive testing reveals a high prevalence of primate bushmeat in Gabon. 9(1): simian T-lymphotropic virus type 1 antibodies 28. in wild adult chimpanzees of the Taï National Liégeois F, Boué V, Butel C, Mouinga-Ondémé A, Park, Côte d'Ivoire. Sica J, Zamba C, Peeters M, Delaporte E, Rouet,

20 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

F (2013). HIV type-1 group O infection in Lord VR, Lord RD (1991) Brucella suis gabon: Low prevalence rate but circulation of infections in collared peccaries in Venezuela. genetically diverse and drug-resistant HIV 27(3): 477-481 type-1 group O strains. Lussac G (2010) Approche écologique, 29(7): 1085-1090 épidémiologique et genetique de la Liégeois F, Courgnaud V, Switzer WM, Murphy biodiversité de Toxoplasma gondii en zone HW, Loul S, Aghokeng A, Pourrut X, Mpoudi- tropicale humide: exemples du Gabon et de la Ngole E, Delaporte E, Peeters M (2006) Guyane Française. PhD Thesis, Université de Molecular characterization of a novel simian Limoges, Limoges, France. immunodeficiency virus lineage (SIVtal) from Madar CS, Cardile AP, Cunningham S, northern talapoins (Miopithecus ogouensis). Magpantay G, Finger D (2012) A case of 349(1): 55-65 Salmonella gastroenteritis following Liégeois F, Lafay B, Formenty P, Locatelli S, ingestion of raw sashimi. Courgnaud V, Delaporte E, Peeters M (2009) 71(2): 49-50 Full-length genome characterization of a Malaisse F, Parent G (1982) Rodents of the novel simian immunodeficiency virus lineage Miombo woodland area: a nutritional and (SIVolc) from olive Colobus (Procolobus ecological approach. verus) and new SIVwrcPbb strains from 11(4): 211-216 (Piliocolobus badius badius) from the Tai Forest in . Mananga V, Elenga M, Massamba D, Makosso- 83(1): 428-439 Vheiye G, Maloumbi MG, Kinkela T (2015) Étude comparée de la biodisponibilité et de la Liégeois F, Lafay B, Switzer WM, Locatelli S, valeur nutritionnelle des triacylglycérols des Mpoudi-Ngolé E, Loul S, Heneine W, Delaporte lipides de l’athérure africain (Atherurus E, Peeters M (2008) Identification and africanus) et du céphalophe bleu molecular characterization of new STLV-1 and (Cephalophus monticola). STLV-3 strains in wild-caught nonhuman 84: 14-25 primates in Cameroon. 371(2): 405- 417. Mander M, Ntuli L, Diederichs N, Mavundla K (2007). Economics of the traditional medicine Liégeois F, Schmidt F, Boué V, Butel C, Mouacha trade in South Africa: health care delivery. F, Ngari P, Ondo M, Leroy E, Heeney JL, 189-196 Delaporte E, Peeters, M Rouet F (2014) Full- length genome analyses of two new Simian Martinez GJ (2013) Use of fauna in the Immunodeficiency Virus (SIV) strains from traditional medicine of native Toba (qom) mustached monkeys (C. Cephus) in Gabon from the Argentine Gran Chaco region: an illustrate a complex evolutionary history ethnozoological and conservationist among the SIVmus/mon/gsn lineage. approach. 2:1-43. 6(7): 2880-2898. Mayor P, Baquedano LE, Sanchez E, Aramburu Locatelli S, Lafay B, Liegeois F, Ting N, J, Gomez-Puerta LA, Mamani VJ Gavidia CM Delaporte E, Peeters M (2008) Full molecular (2015) Polycystic Echinococcosis in Pacas, characterization of a simian Amazon Region, Peru. immunodeficiency virus, SIVwrcpbt from 21(3): 456 Temminck's red colobus (Piliocolobus badius Mbaya AW, Ahmed MI, Ibrahim UI, Lamurde KJ temminckii) from Abuko , The (2010) Trichinellosis in African giant rats Gambia. 376(1): 90-100 (Cicetomycs gambianus) in the arid-region of Locatelli S, Liegeois F, Lafay B, Roeder AD, Northeastern, Nigeria. Bruford MW, Formenty P, Noë R, Delaporte E, 1(10): 460-464 Peeters M (2008a) Prevalence and genetic Milner-Gulland E, Bennet EL (2003) Wild meat: diversity of Simian Immunodeficiency Virus the bigger picture. infection in wild-living red colobus monkeys 18(7): 351-357 (Piliocolobus badius badius) from the Taï forest, Côte d’Ivoire: SIVwrc in wild-living Morales MJ, Villa JT (1998) Notas sobre el uso western red colobus monkeys. de fauna silvestre en Catemaco, Veracruz. 8(1): 1-14 73: 127-143

21 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

Motte-Florac E, Bahuchet S, Thomas JMC 19(1) (1993) The role of food in the therapeutics of Oyarekua MA, Ketiku AO (2010) The nutrient the Aka Pygmies of the Central African composition of the African rat. Republic. In: Hladik CM, Pagezy H, Linares OF, 2(6): 318-324 Hladik A, Semple A, Hadley M (eds) Tropical Forests, People and Food: Biocultural Peeters M, Courgnaud V, Abela B, Auzel P, Interactions and Applications to Development, Pourrut X, Bibollet-Ruche F, Loul S, Liegeois F, Man and Series, Unesco-Parthenon, Butel C, Koulagna D, Mpoudi-Ngole E, Shaw Paris, pp. 549–560 GM, Hahn BH, Delaporte E (2002) Risk to human health from a plethora of simian Mouinga-Ondémé A, Caron M, Nkoghé D, Telfer immunodeficiency viruses in primate P, Marx P, Saïb A, Leroy E, Gonzalez JP, bushmeat. 8(5): 451- Gessain A, Kazanji M (2012) Cross-species 457 transmission of simian foamy virus to humans in rural Gabon, Central Africa. Pernet O, Schneider BS, Beaty SM, LeBreton M, 86(2), 1255-1260 Yun TE, Park A, Zachariah T, Bowden TA, Hitchens P, Ramirez CM, Daszak P, Mazet J, Mouinga-Ondémé A, Kazanji M (2013) Simian Freiberg AN, Wolfe ND, Lee B (2014) Evidence foamy virus in non-human primates and for henipavirus spillover into human cross-species transmission to humans in populations in Africa. Gabon: An emerging zoonotic disease in 5:1-10 central Africa?. 5(6):1536-1552 Pinto LCL, Mateus MB, Pires MRS (2012) Nasi R, Brown D, Wilkie D, Bennett E, Tutin C, Conhecimentos e usos da fauna terrestre por Van Tol G, Christophersen T (2008) moradores rurais da Serra do Ouro Branco, Conservation and use of wildlife-based Minas Gerais, Brasil. 37(7): 520-527 : the bushmeat crisis. Secretariat of the Convention on Biological Diversity, Montreal. Pourrut X, Souris M, Towner JS, Rollin PE, and Center for International Forestry Research Nichol ST, Gonzalez JP, Leroy E (2009) Large (CIFOR), Bogor. Technical Series 33: 1-50 serological survey showing cocirculation of Ebola and Marburg viruses in Gabonese bat Nasi R, Taber A, van Vliet N (2011) Empty populations, and a high seroprevalence of forests, empty stomachs? Bushmeat and both viruses in Rousettus aegyptiacus. livelihoods in the Congo and Amazon Basins. 9(1): 159 13: 355–368 Pozio E, Pagani P, Marucci G, Zarlenga DS, Ndembi N, Kaptue L. Ido E (2007) Exposure to Hoberg EP, De Meneghi D, La Rosa G, Rossi L SIVmnd-2 in southern Cameroon: public (2005) Trichinella britovi etiological agent of health implications. 6(3): 16-19 sylvatic trichinellosis in the Republic of Niyi OH (2014) Nutritional and functional Guinea (West Africa) and a re-evaluation of properties of african wild antelope geographical distribution for encapsulated (Antilocapra americana) meat. species in Africa. 4(4): 546-553 35(9): 955-960 Okoye IC, Ozioko KU, Obiezue NR, Ikele BC Radonić, A, Metzger S, Dabrowski PW, Couacy- (2015) Intestinal parasitic fauna and zoonotic Hymann E., Schuenadel L, Kurth A, Mätz- potentials of commonly consumed wildlife. Rensing K, Boesch C, Leendertz FH, Nitsche A 52(3): 195-204 (2014) Fatal monkeypox in wild-living sooty Olival KJ, Islam A, Yu M, Anthony SJ, Epstein JH, mangabey, Côte d’Ivoire, 2012. Khan SA, Khan SU, Crameri G, Wang LF, Lipkin 20(6): 1009-1011 WI, Luby SP, Daszak P (2013) Ebola Virus Rasambainarivo FT (2013) Prévalence Antibodies in Fruit Bats, Bangladesh. d’excrétion de Giardia et Cryptosporidium 19 (2): 270-273 chez les humains, les animaux domestiques Onadeko AB, Egonmwan RI, Saliu JK (2011) et les lémuriens de l’écosystème du Parc Edible amphibian species: local knowledge of National de Ranomafana, Madagascar. Master their consumption in southwest Nigeria and Dissertation, Université de Montréal, Montreal, their nutritional value. Canada.

22 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

Reynolds MG, Carroll DS, Olson VA, Hughes C, Sirén A (2012) Festival hunting by the kichwa Galley J, Likos A, Montgomery JM, Suu-Ire R, people in the Ecuadorian amazon. Kwasi MO, Jeffrey Root J, Braden Z, Abel J, 32(1): 30-50. Clemmons, C. Regnery R, Karem K, Damon IK Smith KM, Anthony SJ, Switzer WM, Epstein JH, (2010) A silent enzootic of an orthopoxvirus in Seimon T, Jia H, Sanchez MD, Huynh TT, Ghana, West Africa: evidence for multi- Galland GG, Shapiro SE, Sleeman JM, species involvement in the absence of McAloose D, Stuchin M, Amato G, Kolokotronis widespread human disease. SO, Lipkin WI, Karesh WB, Daszak P, Marano N 82(4), 746- (2012) Zoonotic viruses associated with 754 illegally imported wildlife products. Ripple WJ, Abernethy K, Betts MG, Chapron G, 7(1) Dirzo R, Galetti M, Levi T, Lindsey PA, Smith T, Earland J, Bhatia K, Heywood P, MacDonald DW, Machovina B, Newsome TM, Singleton N (1993) Linear growth of children in Peres CA, Wallach AD, Wolf C, Young H (2016) Papua New Guinea in relation to dietary, Bushmeat hunting and risk to the environmental and genetic factors. world's mammals. 31:1-25 3(10): 160498. Soares MDCP, Nunes HM, Silveira FAAD, Alves Roger DD, Justin EJ, Francois-Xavier E (2012) MM, Souza AJSD (2011) Capillaria hepatica Nutritional properties of “Bush Meals” from (Bancroft, 1893)(Nematoda) entre populações North Cameroon’s Biodiversity. indígenas e mamíferos silvestres no noroeste 3: 1482-1493 do Estado do Mato Grosso, Brasil, 2000. Samson C, Pretty J (2006) Environmental and 2(3): 35-40 health benefits of hunting lifestyles and diets Solavan A, Paulmurugan R, Wilsanand V Ranjith, for the Innu of Labrador. 31(6): 528- Sing AJA (2004). Traditional therapeutic uses 553 of animals among tribal population of Tamil Sarkis F (2002) Avaliação das condições Nadu. 3(2), microbiológicas de carnes de animais 206-207 silvestres no município de São Paulo. Subramanian M (2012) Zoonotic disease risk Doctoral dissertation, Universidade de São and the bushmeat trade: assessing Paulo, São Paulo, Brasil awareness among hunters and traders in Sarti FM, Adams C, Morsello C, van Vliet N, Sierra Leone. 9(4):471-482 Schör T, Yagüe B, Tellez L, Quiceno MP, Cruz D Swanepoel R, Smit S, Rollin PE, Formenty P, (2015) Beyond protein intake: bushmeat as Leman PA, Kemp A, Burt FJ, Grobbelaar A, Croft source of micronutrients in the Amazon Tri- J, Bausch DG, Zeller H, Leirst H, Braack LEO, Frontier region. 20(4): 22 Libande ML, Sherif R, Stuart T, Thomas G, Scoones I, Melnyk M, Pretty JN (1992) The Janusz T (2007) Studies of reservoir hosts for Hidden Harvest: Wild Foods and Agricultural Marburg virus. Systems. A Literature Review and Annotated 12(13):1847-1851 Bibliography. International Institute for Tappe D, Sulyok M, Riu T, Rózsa L, Bodó I, Environment and Development, London Schoen C, Muntau B, Babocsay G, Hardi R Sidorowicz J (1974) The effect of fire on small (2016) Co-infections in visceral pentastomiasis, populations in Zambia. Democratic . 27: 18-25 22(8): 1333-1339 Silva E, Rosa P, Arruda M, Rúbio E (2005) Thomas JMC (1987) Des goûts et des dégoûts Determination of duffy phenotype of red chez les Aka, Ngbaka et autres (Centrafrique). blood cells in Dasypus novemcinctus and In: Koechlin B, Sigaut F, Thomas JMC and Toffin Cabassous sp. 65(3): G (eds) De la voûte céleste au terroir, du jardin 555-557 au foyer, EHESS, Paris, pp. 489–504 Siren A, Machoa J (2008) Fish, wildlife, and Truman R (2008) Armadillos as a source of human nutrition in tropical forests: a fat gap? infection for leprosy 33:186–193 101: 581-582

23 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

Truppel JH, Reifur L, Montiani-Ferreira F, Lange Birx DL, Folks TM, Burke DS, Heneine W (2004) RR, de Castro RG, Gennari SM, Thomaz-Soccol Naturally acquired simian retrovirus V (2010) Toxoplasma gondii in Capybara infections in central African hunters. (Hydrochaeris hydrochaeris) antibodies and 363(9413): 932-937 DNA detected by IFAT and PCR. Yang D, Dai X, Deng Y, Lu W, Jiang Z (2007) 107(1):141-146 Changes in attitudes toward wildlife and Tsujimoto H, Hasegawa A, Maki N, Fukasawa M, wildlife meats in Hunan Province, central Miura T, Speidel S, Cooper RW, Moriyama EN, China, before and after the severe acute Gojobori T, Hayami M (1989) Sequence of a respiratory syndrome outbreak. novel simian immunodeficiency virus from a 2(1): 19-25 wild-caught African . 341(6242): Yemi OR, Asiru RA, Shokoya DA (2015) Heavy 539-541 Metals (Cd, Pb, Cu, Fe, Cr, Mn, Zn) Contents Tsujimoto H, Hasegawa A, Maki N, Fukasawa M, in Ungulates of Ogun State Agricultural Farm Miura T, Miura T (1989). Sequence of a novel Settlement, Ago-Iwoye, Nigeria. simian immunodeficiency virus from a wild- 6(2): 119-129 caught African Mandrill. 341(6242): 539- 541 Van Borm S, Thomas I, Hanquet I, Lambrecht B, Boschmans M, Dupont G, Decaestecker M, Snacken R, van den Berg T (2005) Highly Pathogenic H5N1 Influenza Virus in Smuggled Thai Eagles, Belgium. 11(5): 702-705 van Vliet N Mbazza P (2011) Recognizing the multiple reasons for bushmeat consumption in urban areas: a necessary step toward the sustainable use of wildlife for food in Central Africa. 16(1): 45-54 van Vliet N, Fa JE Nasi R (2015) Managing hunting under uncertainty: from one-off ecological indicators to resilience approaches in assessing the sustainability of bushmeat hunting. 20(3) Vega MG, Carpinetti B, Duarte J, Fa JE (2013) Contrasts in livelihoods and protein intake between commercial and subsistence bushmeat hunters in two villages on Bioko Island, Equatorial Guinea. 27(3): 576-587 Whitney ES, Beatty ME, Taylor Jr TH, Weyant R, Sobel J, Arduino MJ, Ashford DA (2003) Inactivation of Bacillus anthracis spores. 9(6): 623-627 Wilkie D, Starkey M, Abernethy K, Nstame E, Telfer P, Godoy R (2005) Role of prices and wealth in consumer demand for bushmeat in Gabon, Central Africa. 19: 268–274 Received: 10 March 2017 Wolfe ND, Switzer WM, Carr JK, Bhullar VB, Accepted: 18 April 2017 Shanmugam V, Tamoufe U, Prosser, AT, Torimiro JN, Wright A, Mpoudi-Ngole E, McCutchan FE, Published: 20 April 2017

24 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

25 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

26 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

27 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

28 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

29 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

30 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

31 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

32 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

33 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

34 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

35 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

36 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

37 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

38 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

39 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

40 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

41 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

42 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

43 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

44 van Vliet et al. 2017. Bushmeat and human health: Assessing the Evidence in tropical and sub-tropical forests Ethnobio Conserv 6:3

45