Evidence for post‐depletion sustainability in a mature bushmeat market

The bushmeat trade, or the trade in wild animals for meat, is a primary threat to wildlife and ecosystems in Sulawesi, Indonesia. Hunting for trade and consumption can hasten the local extirpation of vulnerable species, such as fruit bats and the protected babirusa and Sulawesi crested black macaque. This study provides a much‐needed step in understanding the bushmeat trade by describing longitudinal trends in the amount of bushmeat (animal carcasses) observed for sale in markets in North Sulawesi, a particularly biodiversity‐rich area. Surveys were conducted in 10 markets in 2011, 2015, 2018 and 2019. At each market, total counts of all taxa for sale were noted, and encounter rates per market sample were derived to account for variable sampling effort across years and markets. Generalized Linear Mixed Models were used to compare encounter rates across years, months and markets. Our results show that although animal carcasses are still sold in high numbers, there has been an overall decrease between 2011 and 2019, particularly between 2011 and 2018 (encounter rate fell by 99%). However, bats, rats and Sulawesi warty pigs were still present at high levels, indicating a persistent demand for bushmeat in North Sulawesi. The encounter rate of protected taxa for sale was low, but steady throughout the study period. We identified which markets sold the greatest amount of bushmeat to inform future conservation actions and management. Based on our results, the persistent demand for bushmeat in the region, and the continued presence of protected taxa in the markets, we recommend further research to establish the sustainability of the bushmeat trade at its current rate.

Key messagesIn 2016, the Center for International Forestry Research (CIFOR) and the Secretariat of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) developed a handbook to guide parties in the rapid evaluation of bushmeat trade across their borders, to rapidly assess the impacts on local livelihoods of CITES regulations for bushmeat species, and to identify relevant mitigation measures.Between January and June 2016, CIFOR, in coordination with the CITES focal points for Colombia, applied the handbook to Colombia. This involved a systematic review of available literature; consultations with national and regional authorities; semi-structured interviews with experts; field visits; and regional workshops with stakeholders of the bushmeat trade, local authorities and experts.In Colombia, bushmeat trade operates across boundaries of neighboring countries, in places where geography does not allow for proper institutional control. The transboundary trade occurs in a few specific sites across four main trade routes: three of them in the Amazon and one in the Caribbean.The bushmeat species most commonly traded across Colombian borders are listed in the CITES Appendices: paca, agouti, peccaries and turtles; therefore, the application of CITES could generate negative impacts on the livelihoods of people who depend on this trade.Participants of workshops said that despite the development of alternatives, bushmeat trade will continue given the small costs of hunting compared to any other domestic meat production. Also, they pointed out that bushmeat consumption is rooted in local cultures, creating a potential barrier for any alternative activity to replace bushmeat use.CITES needs to differentiate transboundary trade at local scale between communities of neighboring countries (as in Colombia) from the luxury international trade occurring at larger scales (e.g. from Central Africa to Europe, or from West Africa to the United States) to measure the impacts of CITES regulations on local livelihoods.

The drivers of consumer demand for bushmeat are relatively well studied in tropical forest systems, but much less so in savanna areas. This is important because differing ecological and socio‐economic conditions lead to different factors affecting the relationship between local communities and their natural resources. Northern Ghana is an understudied savanna area, with a recognized cross‐border and long‐distant bushmeat trade. Understanding the role of bushmeat in diets is crucial for food security and conservation policies in the region. We surveyed 471 households in two villages in the Upper East region of Ghana, using questionnaires and focus groups, to examine consumer preferences for bushmeat and the socio‐economic factors influencing its consumption. Fourteen bushmeat species were identified as preferred and/or consumed, with the grey duiker ( Sylvicapra grimmia ) and African savanna hare ( Lepus victoriae ) being the most preferred, although preferences differed by village. The prevalence of smaller, resilient species in preference suggests a depletion of the larger bodied mammals typically found in pristine savanna ecosystems. Bushmeat preference was higher in larger, male‐headed households, those engaged in hunting and in Doninga village, where bushmeat and fish were equally preferred. While bushmeat was mainly preferred for its taste, it was eaten irregularly because of availability and affordability. Domestic meat followed a similar pattern, although Kayoro villagers ate it more often. These village‐level differences may relate to differences in access to slightly more wildlife‐rich Protected Areas. Smoked fish was the most preferred protein source, with respondents indicating that small quantities of it can be bought if money is tight, suggesting food insecurity limits access to animal protein. Our findings depict a landscape of depleted wildlife resources and constrained access to animal protein, where bushmeat is sold rather than consumed locally. Policy efforts should prioritize improving access to affordable, sustainable protein sources like fish, to support food security. Better understanding is needed of the ecological impacts of local bushmeat consumption and its role in livelihoods and food security. This could support the design of conservation and development interventions in this resource‐poor area, for a more sustainable and equitable use of natural resources. Read the free Plain Language Summary for this article on the Journal blog.

The trade of bush meat in Oluwo Market, Epe at Epe Local Government Area of Lagos State was investigated. Eleven animal species from three different classes (Amphibia, Reptilia and Mammalia) of vertebrates were found to be commonly used as bush meat. Xenopus muelleri (frog) was the most abundant animal species traded in the market followed by Crocidiora sp (shrew) and Cephalophus maxwelli (antelope) each having a weekly sale of about 30 individuals. Bitis sp (viper), Pelusioscasteneus (turtle) and Varanus niloticus (monitor lizard) were the least abundant traded animals with a weekly sale of eight, ten and ten respectively. Pertaining to ethnozoological uses, different parts of animal species were used to cure diseases, appease witches, prevent accidents, protect against evil and seek marital partner. Other traders (34%) were the highest customers of bush meat followed by the consumers (22%) and the hotel and restaurant owners (22%). Students and researchers (8%) were the lowest group of customers patronizing the bushmeat trade. Analysis of Variance showed that there was no significant difference between nutritional contents of the various bush meat species at (df= 3; P< 0.005). Appreciating the importance of bush meat both economically and ethnozoologically, it is not only imperative to emphasize and educate all stakeholders in this trade the importance of its conservation and sustainable use, but to also offer efforts that would provide alternative source of protein. Given the present trend of exploitation, many wildlife species may undergo local extinction if urgent measures are not taken

Given the important contribution of urban consumption in bushmeat trade, information on bushmeat sales in urban markets can provide valuable insights for understanding the dynamics of this trade and its implications for conservation and food security. We monitored bushmeat traded in the market of Kisangani (the provincial capital of the Province Orientale in the Democratic Republic of Congo) and compared data collected in surveys in 2002 and 2008–2009. In both periods more than two-thirds of the carcasses sold were of rodents and ungulates. From 2002 to 2008–2009 the number of carcasses increased by 44% but the equivalent biomass by only 16% because of a significant decrease in medium-sized species (10–50 kg) and an increase in small species (<10 kg). The number of carcasses of large species increased between the two periods and those of diurnal monkeys increased fourfold. In both periods smoked bushmeat was one of the cheapest sources of protein available year-round, together with caterpillars, which were only available during the rainy season, and pork. Prices of other domestic meat were significantly higher. This study identified an increase in the market of highly threatened species such as okapiOkapia johnstoniand small diurnal monkeys and the continued presence of protected species, and also highlights the food security role that bushmeat plays for poor urban people who cannot afford alternative sources of protein.

Across West and Central Africa, wildlife provides a source of food and income. We investigated the relation between bushmeat hunting and household wealth and protein consumption in 2 rural communities in Bioko Island, Equatorial Guinea. One village was dedicated to commercial hunting, the other trapped game primarily for food. We tested whether commercial-hunter households were nutritionally advantaged over subsistence-hunter households due to their higher income from the bushmeat trade and greater access to wild-animal protein. We conducted bushmeat-offtake surveys in both villages (captures by hunters and carcasses arriving to each village). Mammals (including threatened primates: black colobus [Colobus satanas], Preussi's guenon [Allochrocebus preussi], and russet-eared guenon [Cercopithecus erythrotis]), birds, and reptiles were hunted. The blue duiker (Philantomba monticola), giant pouched rat (Cricetomys emini), and brush-tailed porcupine (Atherurus africanus) contributed almost all the animal biomass hunted, consumed, or sold in both villages. Monkeys and Ogilbyi's duikers (Cephalophus ogilbyi) were hunted only by commercial hunters. Commercial hunters generated a mean of US$2000/year from bushmeat sales. Households with commercial hunters were on average wealthier, generated more income, spent more money on nonessential goods, and bought more products they did not grow. By contrast, households with subsistence hunters spent less on market items, spent more on essential products, and grew more of their own food. Despite these differences, average consumption of vegetable protein and domestic meat and bushmeat protein did not differ between villages. Our results highlight the importance of understanding the socioeconomic and nutritional context of commercial and subsistence bushmeat hunting to correctly interpret ways of reducing their effects on threatened species and to enable the sustainable offtake of more productive taxa.

Potential environmental and wildlife sources of microorganisms in meat

DNA-typing improves illegal wildlife trade surveys: Tracing the Cameroonian bushmeat trade

Wild animal trade for human consumption is a global issue, involving complex interactions between economics, culture, food security and conservation. Whilst being a biodiversity issue, it is also a major public health concern, with recent epidemics and pandemics of zoonotic pathogens linked to interactions with wildlife. At three time points, between March 2017 and June 2018, a longitudinal sero-survey of 150 market vendors from three wet markets in Laos (selling vegetables, domestic animal meat and/or wildlife meat) was conducted to determine if vendors had been differentially exposed to three endemic bacterial pathogens – Orientia tsutsugamushi, Rickettsia typhi, and Leptospira spp. A total of 367 serum samples were tested by IgG enzyme-linked immunosorbent assay (ELISA) and immunofluorescence assay (IFA, for scrub typhus group (STG) and typhus group (TG) only). Among vendors, 32.7% were IgG-positive for at least one pathogen, 13.3% sero-converted during the study. Multi-season occupancy modelling for STG indicated a significantly higher prevalence of STG IgG in vegetable vendors (27.3%) and wildlife vendors (28.4%) than in domestic animal meat vendors (6.9%, p = 0.05), and higher in Phonsavanh market (OR = 9.6, p = 0.03) compared to Lak Sao and Salavan markets. Estimated mean incidence was 57 cases per 10,000 per 7.5-month period. For TG, vendor age had a significant effect on prevalence (OR = 1.04, p = 0.006), estimated mean incidence was 64 cases per 10,000 per season (7.5-month period). Despite individuals selling domestic meat having a higher prevalence of Leptospira infections than those that did not (11.6% versus 4.5%), the difference was not significant. Whilst this study has a number of limitations, including vendors changing what food types they sold and no investigation of exposure outside of markets, the finding that the risk of exposure of vendors to zoonotic pathogens may be associated with types of food sold for human consumption warrants further investigation.

Our understanding of the linkages between the bushmeat trade and the wider informal economy is limited. This lack of knowledge is particularly problematic for conservation under conditions of political instability, when the informal economy can be highly dynamic and impacts on wildlife populations can be severe. To explore these interlinked processes, we conducted a study of the bushmeat trade in Garamba National Park, Democratic Republic of Congo, through a combination of market surveys, semistructured interviews, and direct observation. We focused on the sale of protected and unprotected species in urban and rural markets, and the bushmeat commodity chains that supplied these markets, under conditions of political stability and armed conflict. During peacetime, protected species from the park (predominantly elephant and buffalo) rarely appeared in the rural markets, but they comprised more than half of all bushmeat sales in the urban markets. This pattern reflected differences in the rural and urban commodity chains. Automatic weapons were urban trade. The use of such weapons was discouraged by the traditional chiefs, who administered the village markets. During wartime, the sales of protected species in the urban markets increased fivefold because the military officers fled, leaving behind an open-access system that led to a massive increase in the exploitation of protected species. In contrast, the rural markets remained relatively stable because of the continued authority of the village chiefs. Our results indicate that sociopolitical factors can be an important determinant of species offtake and, therefore, that knowledge of the bushmeat commodity chain can be vital to controlling theprocesses that drive species extraction. In addition, our findings suggest that traditional authorities can be potentially valuable partners for bushmeat management.

The trade of bushmeat from rural areas to supply burgeoning cities is a major conservation and livelihood concern. Using a whole-city sampling strategy we mapped the distribution and numbers of meat outlets in the Kinshasa–Brazzaville metropolitan area, two neighboring capital cities in Central Africa. We show that both cities differ in the number and density of meat outlets, with more in Brazzaville per area sampled and inhabitants. The number of meat outlets is related to human population densities and primarily concentrated along the banks of the Congo River, in the more affluent areas of the cities. Across the two cities, roughly 22% of all sampled markets (50% in Brazzaville and 19% in Kinshasa) and 24% of all visited restaurants (24% in each city) were selling bushmeat during our survey. Despite the relatively low number of establishments offering bushmeat for sale, extrapolated to the entire area and population of both cities, we expect the overall amount of wild animal meat consumed per annum to be significantly high. We suggest that the supply of such numbers of wild animal meat will strongly impact the animal populations sourcing these cities. Our data also indicate that the number of domestic meat outlets may be adequate to supply urban dwellers with sufficient animal protein.

Illegal bushmeat trade is a significant driver of the decline in wildlife populations within the tropics. Despite the intense trade of bushmeat in Cameroon, there is dearth or no official statistics on the kind of animals sold in the markets in most parts of Cameroon. To abridge this knowledge gap, an inventory of wild animals sold in local markets was carried out. The animal taxa sold within the markets were identified, and their abundance, class diversity and conservation status according to the IUCN Red List of threatened species and Cameroon wildlife classification were assessed. Semi‐structured questionnaires were randomly administered to 200 traders randomly selected in 16 markets. Multivariate analyses were used to compare the proportions of sold taxa among the markets and the proportions of taxa based on their conservation status. Results were summarized as shown below: (1) 476 individuals of animals were recorded, covering 47 taxa, 41 genera, 33 families, 18 orders and 3 classes from bushmeat vendors. (2) Mammals dominated the trade in all markets (by a mean of 74.3% per market), followed by reptiles (16.1%) and birds (9.5%) in terms of both abundance and diversity. (3) Cane rats (Thryonomyidae) and primates (Cercopithecidae) represented the highest proportions of animal specimens recorded. (4) The diversity of mammals sold was highest in Foumbot, followed by Bangangte, Bafousam and Bangoua as the main local markets, and lowest mammalian diversity was found in Batcham and Baham village markets. (5) The most often traded animal species belonged to the least concern category, followed by vulnerable, near threatened, endangered, and critically endangered. In general, we observed that less protected species by the IUCN Red List and Cameroon wildlife classification were often found in village markets and species with higher conservation value were often sold in city markets. Similarly, the main markets hosted the highest diversity of sold animals, especially mammals. The size of the human settlement together with its location nearby protected area and/or placement of the market by the main road are the main drivers determining numbers and diversity of sold animals, and further attention to government conservation activities should be focused on these markets.

Determinants of urban bushmeat consumption in Río Muni, Equatorial Guinea

A multiplex PCR method to identify bushmeat species in wildlife forensics

Understanding the patterns of wild meat consumption from tropical forests is important for designing approaches to address this major threat to biodiversity and mitigate potential pathways for transmission of emerging diseases. Bushmeat consumption has been particularly poorly studied in Madagascar, one of the world's hottest biodiversity hotspots. Studying bushmeat consumption is challenging as many species are protected and researchers must consider the incentives faced by informants. Using interviews with 1154 households in 12 communes in eastern Madagascar, as well as local monitoring data, we investigated the importance of socio-economic variables, taste preference and traditional taboos on consumption of 50 wild and domestic species. The majority of meals contain no animal protein. However, respondents consume a wide range of wild species and 95% of respondents have eaten at least one protected species (and nearly 45% have eaten more than 10). The rural/urban divide and wealth are important predictors of bushmeat consumption, but the magnitude and direction of the effect varies between species. Bushmeat species are not preferred and are considered inferior to fish and domestic animals. Taboos have provided protection to some species, particularly the Endangered Indri, but we present evidence that this taboo is rapidly eroding. By considering a variety of potential influences on consumption in a single study we have improved understanding of who is eating bushmeat and why. Evidence that bushmeat species are not generally preferred meats suggest that projects which increase the availability of domestic meat and fish may have success at reducing demand. We also suggest that enforcement of existing wildlife and firearm laws should be a priority, particularly in areas undergoing rapid social change. The issue of hunting as an important threat to biodiversity in Madagascar is only now being fully recognised. Urgent action is required to ensure that heavily hunted species are adequately protected.