Local hunting of carnivores in forested : a meta-analysis

H UNTER L. DOUGHTY,SARAH M. KARPANTY and H ENRY M. WILBUR

Abstract We conducted a meta-analysis of local hunting impacts, including the effects of local hunting practices. practices affecting the carnivores of forested Africa and Examples are the unsustainable hunting of Cryptoprocta Madagascar to collate the information available on this subject ferox in north-east Madagascar (Golden, ), local extinc- and to assess underlying trends in offtake rates. We located  tions of Panthera pardus in various locations, such as south- relevant articles in a detailed literature search; the data in- west Cameroon (Abugiche, ), and local extinctions of cluded taxa reported as hunted, the purpose of hunting and Civettictis civetta at several sites in Ghana (Ryan & the hunting method. The families most reported as hunted Attuquayefio, ). were Herpestidae and Viverridae (excluding Civettictis civet- Carnivores are a keystone species in forest ecosystems ta), with . and .% of total records, with C. civetta com- and so their absence or reduction can distort the trophic bal- prising .% of records and Nandina binotata .%. Hunting ance (Bond, ). If hunters are exploiting these species to for consumption was the most commonly reported purpose fulfil subsistence or revenue needs, then understanding the (.% of all records). Sale for consumption was associated full extent of such actions will enable us to prevent total with .% of all consumption records, and sale of any kind depletion and to plan better for substitute food resources was reported for .%ofallrecords.Thenumberofcarnivore across Africa (Bennett et al., ). carcasses or parts sold at urban markets rose by .%fromthe Our objectives were to assess whether carnivores are stothes. The commonest hunting methods were commonly hunted across the forests of Africa and traps (.% of records) and guns (.%). For records report- Madagascar for reasons beyond simple nuisance control ing the use of guns, .% also reported sale of some kind. We or for their pelts. Our analysis provides a collation and conclude that carnivores are hunted pervasively across the assessment of information on the effect of hunting practices forested regions of mainland Africa and Madagascar, and off- on carnivores. Our focus is on the purpose and means of take rates for both personal use and income are probably hunting, along with the taxa most affected. increasing. These findings have implications for efforts to pro- tect dwindling forest ecosystems and to establish sustainable Methods consumptive practices.

Keywords Africa, , carnivore, hunting, Madagascar, The term used to search for relevant articles included coun-  sustainability tries and carnivore taxa (Supplementary Material ). Google Scholar (Google, Mountain View, USA) was used as the This paper contains supplementary material that can be search engine because it examines all text fields in a found online at http://journals.cambridge.org large array of databases rather than only titles and abstracts. Google Scholar has been used previously for meta-analyses (e.g. Branton & Richardson, ; Lelieveld, ). Each search included the phrases ‘bushmeat’ and ‘bush meat’ Introduction (bushmeat describes any wild animal used for human con-  orested landscapes across mainland Africa and sumption; Bennett et al., ). This search may miss arti- FMadagascar support an exceptionally diverse assem- cles referring to the hunting of carnivores solely for other blage of carnivorous mammals (Happold, ; Ray, purposes, such as cultural ceremonies, or articles that do ). Varying in size, food preference and home ranges, not refer to wild meat as bushmeat. However, through the these carnivores have important ecological roles and yet use of this search and many citation chains we believe that are in most cases poorly known (Ray, ). Despite this, the majority of relevant studies were discovered. The search they are cited in discussions of ever-growing anthropogenic results included studies focused on alternative uses for car- nivores, further suggesting that the search was thorough. Most of the research on local hunting has been referred to HUNTER L. DOUGHTY (Corresponding author) and HENRY M. WILBUR Department as bushmeat hunting and therefore even non-bushmeat of Biology, The University of VA, 229 Gilmer Hall, 485 McCormick Road, Charlottesville, VA, 22904-4328, USA. E-mail [email protected] studies often reference bushmeat research. The final search was completed on  March . SARAH M. KARPANTY Department of Fish and Wildlife Conservation, Virginia  Tech, Blacksburg, Virginia, USA We located and reviewed a total of articles published –  Received  September . Revision requested  November . during (Supplementary Material ). These in- Accepted  February . First published online  October . cluded  reports of the hunting of carnivores. All articles

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were restricted to forest habitats in Africa or Madagascar (Fig. ). Madagascar was included because its carnivores, although taxonomically separate from those of mainland Africa, occupy similar niches and are hunted for similar rea- sons. For a few studies conducted across multiple habitat types, such as whole parks, it was difficult to exclude non- forest locations unless these were clearly distinguished. There was a higher frequency of articles in more recent years, probably a result of increased research efforts and im- proved research techniques. Information was extracted on every carnivore taxon specifically cited by researchers as being hunted within their study area. Each taxon is consid- ered one record in the analysis. The items noted for each rec- ord were: article citation, size class and species of carnivore, purpose of hunting, hunting method, method employed by researchers, political location and habitat of study area. Only primary data, collected using one of the recorded research methods, were included in the analysis (Supplementary Table S). Hearsay records, most books, many non-reviewed conference reports, and references to accounts of earlier explorers where the original publication  could not be located, were discarded. FIG. 1 Locations of study sites (black-filled circles) for the ’ articles (Supplementary Material ) reporting hunting of Size class was determined by a taxon s mean body weight,  ,   ,  .  carnivores across forested areas of Africa, with political defined as small ( kg), meso ( kg) and large ( kg; boundaries. All copyrights of this royalty-free map belong to  Animal Diversity Web, ). Family level groupings d-maps.com, –. (Table ) were formed with the taxonomy used by IUCN (; Supplementary Table S). Civettictis civetta was sepa- were dominated by P. pardus (Table ). A summary of the rated from Viverridae for the purposes of this study because purposes of hunting is given in Table . Consumption com- it is biologically dissimilar from other members of its family. prised the majority of all records and was reported for all Being large, the ecological role of C. civetta is different from its size classes, and was the primary purpose for hunting smaller relatives and it is perceiveddifferently by local hunters. seven of the nine taxonomic groups. Records of C. civetta Its high prevalence in our literature search warrants particular were associated primarily with consumption (.%), and interest. The African palm civet Nandinia binotata belongs to of records reporting consumption .% were for sale, and a monotypic family and, like C. civetta, is of particular inter- of these .% were for urban sale. Records of N. binotata est because of its high prevalence in reports of offtake. were also associated primarily with consumption (.%), Records that could not be classified at the family level as a and of records reporting consumption .% were for sale, result of vagueness in identification were not included in and of these .% were for urban sale. family level analyses. The majority of records of consumption were of The variables hunting purpose and method, and research Herpestes, followed by species of viverrids and C. civetta. method, were not mutually exclusive. Data were presence/ Cultural use was the second most commonly reported pur- absence and a record could be included in multiple categories. pose, with herpestids and then viverrids the most commonly For example, if a researcher used market surveys and hunter reported families. Nearly a third of the records of large car- interviews then both would be tallied under research method. nivores were taken for cultural purposes (Table ). The Recorded purposes for hunting are giveninSupplementary highest percentage involved herpestids and then viverrids. Table S: consumption, culture (use other than as food), pest Cultural uses were recorded for . % of all observations (unwanted animals, such as nuisance species), and for five out of the nine groups. Twelve of  purpose obser- unknown (reason for hunting not specified). The hunting vations of the large-size class were for cultural use. Sale for methods recorded are given in Supplementary Table S. fetish uses comprised .% of all reports for cultural use. Pest control was the third most frequently reported reason Results for hunting, with felids most commonly reported for this purpose, followed by viverrids and mustelids. N. binotata Records involving small carnivores were dominated by her- was not hunted as a pest. Records reporting sale of any pestids and viverrids. Meso carnivores were dominated by kind (consumption, fetish or unknown) composed .% C. civetta. Large carnivores, such as felids and hyaenids, of all  purpose observations. Carnivores taken for sale

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TABLE 1 Number of reports of the hunting of carnivores (of a total of  reports) in  studies (see text for details), by family (Civetta civetta and Nandinia binotata are treated as separate groups for the purpose of this analysis; see text for further details) and size class (see text for details), with number and percentage of total records for each group.

Frequency Small Meso Large Family (, 6 kg) (6 , 23 kg) (. 23 kg) Total no. % Canidae 3 3 0.9 C. civetta 45 45 13.5 Eupleridae 8 8 2.4 Felidae 14 6 25 45 13.5 Herpestidae 109 109 32.7 Hyaenidae 2 2 0.6 Mustelidae 24 24 7.2 N. binotata 33 33 9.9 Viverridae 64 64 19.2 Total (%) 231 (68.6) 79 (23.4) 27 (8.0)

were sold for consumption (.% of all reports of animals Discussion taken for sale and .% of all animals taken for a reported purpose) and for fetish use (.% of all reports of animals Pest taken for sale and .% of all animals taken for a reported purpose). Personal consumption was reported in  Pest control was in general not the sole reason reported for records and consumption for sale in  records. Of the killing carnivores. Even in areas where carnivores were con- sales records .% were for local sale and .% for sidered village marauders and poultry killers, they were also  urban sale. Herpestidae (.%) and Viverridae (.%) con- still considered a protein source (Campbell, , Ghana;   tributed most to records of sale in urban areas. Sale in urban Djagoun & Gaubert, , Benin; Kotschwar et al., , areas for reports published between  and  is shown Madagascar). Where nuisance was the sole reason  by decade in Fig. . Of the  records for urban sale,  are reported (e.g. Carpaneto & Fusari, ), species were not from studies conducted in the s and the s. eaten because it was either taboo to do so or they were The numbers of reports by hunting method are pre- poor tasting. sented in Fig. . Traps were the most popular hunting meth-     od ( . % of records), followed by guns ( . %). Traps were Culture the primary method of hunting for five of the nine groups. However, for the other four groups, N. Binotata was Nearly a quarter of records that gave reasons for taking reported as taken equally by guns and traps, and Canidae, carnivores reported cultural uses, primarily as skins or in Hyaenidae and Felidae were all reported as being taken by fetish practices. Uses of fetish products for spiritual vs medi- unknown methods more frequently than by traps. cinal practices are often difficult to distinguish. For example, There were only  reports of night hunting but .%of skins of genets, civets, and felids are used in utilitarian and these were from records associated with sale for consump- ornamental fashions (Maisels et al., ). The Mbuti people tion, and .% were for urban sale for consumption of the Democratic Republic of the Congo (DRC) use genet (Table ). Only two reports of night hunting did not also and civet skins in wrist guards for archery and for hats used report the use of guns. Of the  reports of the use of in initiation ceremonies (Carpaneto & Germi, ). guns, .% also reported sale of some kind. Additionally, Genetta servelina and Genetta pardina skins are used as a .% of all sale reports were associated with use of guns, mark of importance in Cameroon (Pollard, ). Genets and .% of reports of urban sale for consumption were as- are used as medicine in Ghana (Ntiamoa-Baidu, ), the sociated with the use of guns. oil from C. civetta glands is used against respiratory pro- Carnivores specifically defined by the original authors as blems in Cameroon (Laurent, ), and Crossarchus rare but still hunted totalled  reports in eight articles. obscurus, and Herpestes ichneumon are used in animist Carnivores specifically defined as locally extinct totalled  rituals in Benin (Djagoun & Gaubert, ). In Nigeria reports in seven articles. Civettictis civetta was the carnivore leopard parts are believed to increase fertility, protect most recorded as rare and P. pardus was the carnivore most against or invoke witches, and to counter snake venom recorded as locally extinct (Supplementary Table S). (Sodeinde & Soewu, ). Otters are used in Tanzania as

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are treated as separate groups for the FIG. 2 Percentage of all records within a given decade that reported urban sale of carnivores for consumption. N. binotata and fic to be included in the family level analysis but were included in the C. civetta

FIG. 3 Number of reports (of a total of )in articles (Supplementary Material ) of the hunting methods used for carnivores.

medicine and belt buckles (De Luca & Mpunga, ), and in Central and West Africa otter fur is believed to render the bearer invisible to enemies (Jacques et al., ). Many supposedly protected carnivores used in tradition- al medicine are commonly and openly sold throughout West Africa. Ntiamoa-Baidu () notes that carnivore parts are sold for traditional medicine in at least one location in all major towns in West Africa. Sodeinde & Soewu () found that % of fetish market stalls in Nigeria carried the protected serval Leptailurus serval. Hunters in southern Benin use fetish markets as their primary means for selling small carnivores, especially N. binotata, Lutrinae and Viverridae (Djagoun & Gaubert, ). This prevalence of sales for fetish purposes implies animals once used within a family or village for local traditions are now sold at a region- al scale, suggesting a large network of trading for this pur-

42 71.233 14 78.6 13 11pose 22 and 7growing 11.3 demand. 16.7 2 6.1 3.4 0 5.1 0 2 0 3.4 2 6.1 4.8 6.1 Consumption Culture297 (61.6)301 (61.7) Pest 115 (23.9) 115 (23.6) Unknown 37 (7.7) 39 (8.0) 33 (6.8) 33 (6.8)

Consumption

2 Number of reports of the purpose of hunting (for consumption, cultural use, as a pest, or unknown) by family ( Consumption was the most frequently reported reason for hunting but it is difficult to determine who is consuming ABLE overall analyses. T *Total number of reports differs between the family and overall because some reports (such as those for small carnivores) were not sufficiently speci Family groupingCanidae No.C. civetta EupleridaeFelidaeHerpestidae % ofHyaenidae group 1Mustelidae 7 % ofN. use binotata 105Viverridae 29 No.Family total 33.3 (%) 0 21Overall total (%)* 63.6 69.1 % 59 of 47.5 group 0.3 0 % 43.8 of use 2.3 34.9 No. 56.7 9.6 0 7 31 0 0 % of group 19 19.6 % of use 0 20.4 15 0 No. 1 29 31.2 % of 31.3 27 group 0 50 27.9 0 16.5 % of use 13 7 2 9 25.2 3 0.9 66.7 4.6 6 14.8 7 27.3 1 12.5 18 5.1 23.1 6.7 50 7.7 0 4 15.4 9 1 18 2.6 6 0 6.6 5.9 9 9.1 0 12.5 12.1 27.3 0 8.7 3 0 18.2 27.3 0 purpose of this analysis; see text for further details), with the percentage of reports within a group and percentage of reports within a use type. the meat. Some areas have a religious prohibition against

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TABLE 3 Number of reports of carnivores in which night hunting or gun use is given as the hunting method, and sale of any kind is given as the hunting purpose, showing affiliations between these hunting methods and hunting for profit.

All sale types1 Sale for consumption2 Sale for urban consumption n Row % Column % n Row % Column % n Row % Column % Night 18 64.3 6.5 18 64.3 7.9 12 42.9 11.1 Guns 143 89.4 51.8 116 72.5 51.1 52 32.5 48.2

 Includes sale for consumption, sale for fetish uses, and unknown uses.  Includes records reporting sale for consumption through local, urban, or unspecified markets.

eating certain carnivores whereas in other areas the same viverrids; Martin, ), , % (Kümpel, ), and % species command high prices. Taboos preventing hunting (Keylock, ). At the other extreme, Kümpel () listed of various carnivores were present in areas such as N. binotata and G. servalina as two of the most frequently Equatorial Guinea (Keylock, ), Republic of the Congo seen species at market. Bushmen of south-east Nigeria (Mbete et al., ) and Madagascar (Kotschwar et al., in traded carnivores and artiodactyls more than any other press). Many taboos referred to pregnant women. Genets animal type (Angelici, ), and Atilax paludinosus was in Cameroon, for example, are said to cause mother and one of the six most expensive meats per unit mass in eastern child to catch a cough, and C. civetta to cause a child to Cameroon (Tieguhong & Zwolinski, ). Carnivores be born with body odour (Ayeni et al., ). In DRC appear to be increasingly sold in urban areas. Bassett both N. binotata and C. civetta are thought to cause devel- () reported that carnivores increased in the bushmeat opmental anomalies in children (Carpaneto & Germi, ). trade in northern Côte d’Ivoire from his first survey in Taboos can also have a spiritual basis. Where leopards are – to his second in –. This increase was considered a totem animal, villagers believe they can trans- attributed to depletion of other wildlife, especially of large, form into totem species, and therefore killing a leopard preferred herbivores. These examples support the notion could kill the totem’s owner (Nzouango & Willcox, ; that as preferred species are depleted a general shift of trade Abugiche, ; Wright & Priston, ). towards less desired animals, including carnivores, is likely. Although taboos may protect carnivores, the belief that physical and mental ailments are associated with meat intake may be applicable only to a gender or age group, Hunting methods such as child-carrying women. These beliefs are waning (Nzouango & Willcox, ; Wright & Priston, ) The hunting method was unknown for .% of reports because of increased interaction with outside education (Supplementary Table S). For known hunting methods and beliefs (Sifuna, ), and perhaps from an increased however, trapping, predominantly by snares, was the most need for meat or money. frequent catch technique (Nzouango & Willcox, ;Fa Of reports of consumption .% cited immediate per- & Yuste, ; Golden, ). Trapping may be indiscrim- sonal use. Noss (), Vliet & Nasi () and Keylock inate, capturing any species, but Abugiche () found that () noted that carnivores are often kept and eaten within snares selectively trap C. obscurus, and Fa & Yuste () the hunter’s family. Carnivores are also eaten in the forest found that carnivores were particularly vulnerable to snares, during extended hunting trips (Kümpel, ) because suggesting that the discrimination of a trap may depend on they are less favoured by traders and buyers (Noss, ; its design and/or placement. Nzouango & Willcox, ). Personal consumption of Guns were the hunting method in .% of reports. Use carnivores could negatively affect carnivore populations in of guns is currently expanding to locations such as forested Africa if these less desirable animals are a major Cameroon (Willcox & Nambu, ), Guinea (Ziegler food source for the hunter and his family. Halle () et al., ) and Ghana (Crookes et al., ). The percent- reported that in South America the more desirable meat age of carnivores killed with a shotgun rose from c. %in goes to market and the less favoured meat stays within the  to c. %in in Equatorial Guinea (Gill, ). hunter’s family, which invariably results in the ‘urban This rise was attributed to an increase in income, enabling markets indirectly generat[ing] additional pressure on less more hunters to afford guns and cartridges. Similarly, preferred species.’ Kümpel () argued that waxing accessibility to guns Carnivores compose a small but consistent portion of a and waning trapping success caused hunters to transition hunter’s total sales, with .% of reports of consumption from traps to guns. Over half of all reports of sale of bush- associated with sale. Examples of the percentage of carni- meat for consumption were associated with guns, and vores of total sales are: .% (Juste et al., ), .% (all almost % of all gun reports were associated with sale of

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some kind, suggesting that guns are being employed almost sold in markets (Kümpel, ), where it is also the only exclusively where hunting is for profit. If hunting for sale is carnivore commonly sold (Foerster et al., ), and why it increasing, the percentage of hunters with guns will prob- is one of the most expensive (Gill, ). Although N. bino- ably also increase. tata is considered a common species in many places,  of Night hunting (jacklighting), in which a hunter uses a the  studies within the species’ range (IUCN, ) did not light to halt an animal and shoot it (Hennessey & Rogers, report it as present, suggesting it is also undergoing localized ), was reported in .% of records. Hunters in the depletion. Republic of the Congo reported jacklighting as one of the Although Herpestidae account for a high percentage of easiest means of hunting, and civets as one of the two records, harvest relative to other carnivores may be inflated main animals targeted (Hennessey & Rogers, ). because of the high numbers of this family in a given study Likewise, hunters in Gabon reported night hunting as area. Three herpestids (marsh mongoose A. paludinosus, being more efficient and that small nocturnal carnivores black-footed mongoose B. nigripes and dwarf mongoose such as C. civetta, N. binotata, Bdeogale nigripes and C. obscurus; Laurent, ; Pollard, ; Puit et al., ) Poiana richardsoni are mostly killed this way (Vliet & comprised .% of all records. Mongoose species are com- Nasi, ). About % of all night hunting records were monly hunted (Lupo & Schmitt, ; Carpaneto et al., associated with sale. This is not as strong an association as ) but it is not easy to assess any impact because hunters with all gun methods but rising sales would logically lead to are unaware of species distinctions and because of the diffi- increased night hunting, for if hunters are transitioning to culty in identifying smoked or butchered specimens. seeking smaller prey then more profitable hunting methods The family Viverridae (excluding C. civetta) presents would be desirable. similar uncertainties:  of  references to the genus Government curbs on these hunting methods may be Genetta were for ‘genet species’, and genets are often effective in many locations but appear readily ignored in grouped together as one taxon. This is doubtless because others. Snares, although illegal, are the most popular method these often solitary, – kg species are frequently mistaken of hunting in the Republic of the Congo (Hennessay & Rogers for one another (Nowak, ). Regardless of this uncer- (). Vermeulen et al. () reported snaring, guns, and tainty, species of Genetta were observed in many studies. night hunting as illegal, but used commonly. Wilkie et al. Genetta servalina, the most reported species, was noted as () noted that illegal jacklighting and non-traditional the most frequently sold species in at least one location. snares are ‘openly employed and are acknowledged as the The families Felidae and Mustelidae appear to be com- most common, preferred, and effective techniques’. monly hunted, and the most hunted felid is the Near Threatened leopard. No species of Mustelidae represented  Taxa affected by hunting more than % of total records but species of the subfamily Lutrinae are commonly used for cultural purposes. There Civettictis civetta is thought to be widely distributed through- are relatively few records of the family Eupleridae, found out forested Africa and is categorized as Least Concern on the solely in Madagascar, being hunted. IUCN Red List (IUCN, ), although it is commonly taken for sale of its musk to the perfume industry. The relatively Conclusions large size of this civet (– kg), and its terrestrial habits, make it a desirable and easy target (Carpaneto & Germi, Biases in this analysis potentially arise from the keywords ). Laurent (), Lupo & Schmitt (), and Mbete used in the search and non-random coverage in the litera- et al. () report that it is one of the most commonly hunted ture of the topics we address. Most studies of localized hunt- species. Carpaneto & Fusari ()foundthatC. civetta is the ing concern bushmeat and therefore most articles report the only animal to be eaten in hunting of nuisance animals in purpose of take to be for consumption. Only a few studies Tanzania. Djagoun & Gaubert () noted the high resale focused primarily on cultural uses. However, research that value of C. civetta in the fetish markets of southern Benin. included structured interviews, questionnaires or anecdotal In addition to the five occurrences of known rarity for C. ci- information documented additional non-consumptive pur- vetta and one of local extinction (Supplementary Table S),  poses for hunting carnivores. Our meta-analysis suggests, studies within the species range (IUCN, ) failed to report nevertheless, that carnivores are hunted pervasively across it, suggesting that this presumed widespread species is under- forested Africa. Research on hunting therefore needs to con- going localized depletion. sider carnivores in more detail. In addition, as much hunt- The Least Concern N. binotata (IUCN, ) is an easy ing is for personal uses (consumption, culture or pest target for hunters because of its conspicuousness and gre- control), information needs to be gathered on carnivores gariousness (Okiwelu et al., ). Hunters net large num- not intended for sale. bers of this frugivore as they descend from fruiting palms. The impacts of hunting on carnivores affect not only the This may explain why it is one of the most common species assemblage of species to which these animals belong but also

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have implications for the people causing these impacts. If conservation. Mustelid and Viverrid Conservation; The Newsletter local hunters continue to use carnivores for subsistence or of the IUCN/SSC Mustelid and Viverrid Specialist Group, , –.  revenue then it is imperative that we understand the sustain- CROOKES, D.J., ANKUDEY,N.&MILNER-GULLAND, E.J. ( ) The value of a long-term bushmeat market dataset as an indicator of ability of such actions, to prevent a collapse of food supply system dynamics. Environmental Conservation, , –. should this resource become exhausted. DE LUCA, D.W. & MPUNGA, N.E. () Carnivores of the Udzungwa The effects of hunting on the carnivores of forested Mountains: Presence, Distributions and Threats. Wildlife Africa appear to be escalating and remain poorly under- Conservation Society, Mbeya, Tanzania.  stood. The notion that carnivores are hunted solely for DJAGOUN, C.A.M.S. & GAUBERT,P.( ) Small carnivorans from southern Benin: a preliminary assessment of diversity and hunting pest control is untenable, the taboos preventing their use pressure. Small Carnivore Conservation, , –. as food are deteriorating, and there is a lack of conservation FA, J.E. & GARCÍA YUSTE, J.E. () Commercial bushmeat hunting attention to their increased use for both personal consump- in the Monte Mitra Forests, Equatorial Guinea: extent and impact. tion and sale for consumption. Animal Biodiversity and Conservation, , –. FOERSTER, S., WILKIE, D.S., MORELLI, G.A., DEMMER, J., STARKEY, M., TELFER, P. et al. () Correlates of bushmeat hunting among Acknowledgements remote rural households in Gabon, central Africa. 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