Trade of Threatened Vultures and Other Raptors for Fetish and Bushmeat in West and Central Africa

Trade of threatened vultures and other raptors for fetish and bushmeat in West and Central Africa

R. BUIJ,G.NIKOLAUS,R.WHYTOCK,D.J.INGRAM and D . O GADA

Abstract Diurnal raptors have declined significantly in Introduction western Africa since the s. To evaluate the impact of traditional medicine and bushmeat trade on raptors, we ex- ildlife is exploited throughout West and Central  amined carcasses offered at markets at  sites (– stands WAfrica (Martin, ). The trade in bushmeat (wild- per site) in  countries in western Africa during –. sourced meat) has been recognized as having a negative im- Black kite Milvus migrans andhoodedvultureNecrosyrtes pact on wildlife populations in forests and savannahs    monachus together accounted for %of, carcasses com- (Njiforti, ; Fa et al., ; Lindsey et al., ), and it .  prising  species. Twenty-seven percent of carcasses were of is estimated billion kg of wild animal meat is traded an-  species categorized as Near Threatened, Vulnerable or nually in Central Africa (Wilkie & Carpenter, ). In add- Endangered on the IUCN Red List. Common species were ition to being exploited for bushmeat, many animals are traded more frequently than rarer species, as were species hunted and traded specifically for use in traditional medi-  with frequent scavenging behaviour (vs non-scavenging), gen- cine, also known as wudu, juju or fetish (Adeola, ). eralist or savannah habitat use (vs forest), and an Afrotropical The use of wildlife items for the treatment of a range of (vs Palearctic) breeding range. Large Afrotropical vultures physical and mental diseases, or to bring good fortune, were recorded in the highest absolute and relative numbers has been reported in almost every country in West and in Nigeria, whereas in Central Africa, palm-nut vultures Central Africa. Birds, mammals, reptiles and other taxa Gypohierax angolensis werethemostabundantvulturespe- are sold at specialized fetish markets. However, many species. Estimates based on data extrapolation indicated that cies are sold for fetish alongside those sold for their meat, within West Africa % of carcasses were traded in Nigeria, or they are sold for either purpose, suggesting that the trad- %inBeninand% elsewhere. Offtake per annum in West itional medicine and bushmeat trades are probably inte- Africa was estimated to be –, hooded vultures, – grated and to some extent interdependent (Saidu & Buij,   palm-nut vultures, – Rüppell’sgriffonsGyps rueppellii, ; Williams et al., ). In urban settings the commercial – African white-backed vultures Gyps africanus, – trade in wildlife-based medicinal products is often concen- lappet-faced vultures Torgos tracheliotos,and– crowned trated in traditional markets, where various animals, includ- eagles Stephanoaetus coronatus.Thisrepresentsasizeable ing threatened species, are offered openly for sale. In a few proportion of regional populations, suggesting that trade is countries such practices have become uncommon, but in likely to be contributing significantly to declines. Stronger Burkina Faso and Benin they represent a strong cultural commitment is needed, especially by governments in tradition that is supported by the governments of these  Nigeria and Benin, to halt the trade in threatened raptors countries (Nikolaus, ). and prevent their extirpation. The commercialization of biological resources often has important conservation implications for heavily exploited spe- Keywords Bushmeat, commercial trade, diurnal raptors, cies, especially those under pressure from other anthropogenic traditional medicine, vultures, West and Central Africa factors, such as habitat loss (Alves et al., ). This is the case To view supplementary material for this article, please visit in many parts of West and Central Africa, where human http://dx.doi.org/./S population densities and growth rates are high, even by sub-Saharan African standards. Increases in human populations contribute to high rates of land-use change and exploitation of wildlife, which also occurs frequently in protected R. BUIJ (Corresponding author) Alterra, Wageningen University and Research Centre, PO Box 47, 6700 AA Wageningen, The Netherlands areasintheseregions(Brasharesetal.,;Newmark, E-mail [email protected] ). Large, long-lived apex predators with low productivity G. NIKOLAUS Feldweg 87, Cuxhaven, Germany and slow maturation rates, such as large raptors, are especially

R. WHYTOCK School of Biological and Environmental Sciences, University of vulnerable to increases in mortality rates, which can have a Stirling, UK significant impact on population viability (Sæther & Bakke, D. J. INGRAM School of Life Sciences, University of Sussex, Brighton, UK ). Given such vulnerability, increasingly intense persecu-

D. OGADA* The Peregrine Fund, Boise, Idaho, USA tion and hunting pressure related to commercial trade was *Also at: National Museums of Kenya, Ornithology Section, Nairobi, Kenya suggested as one of the major drivers of the widespread de- ’ Received  August . Revision requested  December . cline of vultures (i.e. Rüppell s Gyps rueppellii,white-backed Accepted  April . First published online  August . Gyps africanus, lappet-faced Torgos tracheliotus,white-headed

Oryx, 2016, 50(4), 606–616 © 2015 Fauna & Flora International doi:10.1017/S0030605315000514 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.14, on 30 Sep 2021 at 03:19:52, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605315000514 Threatened raptors in Africa 607

FIG. 1 Locations of the  markets in West and Central Africa where surveys of raptor carcasses for sale were conducted during – (Supplementary Table S). Biomes are based on White ().

Trigonoceps occipitalis, and hooded vultures Necrosyrtes mon- component of traditional medicine in the region, we deter- achus) in the savannah biome during – (Thiollay, mined the overall contribution of vultures to the total number , ; Rondeau & Thiollay, ). Although a variety of raptor carcasses recorded, and examined temporal changes of techniques are used to kill vulturesandotherraptorsfor therein. We also evaluated changes in the proportion of black traditional medicine and consumption (Buij & Croes, ), kites Milvus migrans among carcasses, because these relative- the use of poisoned baits is probably the most widespread ly common raptors are used regularly as substitutes for vul- method,oftenkillingmanyvulturesinasinglelocation tures by fetish traders, who pluck feathers from the kites’ (Mander et al., ;Saidu&Buij,). heads so that they resemble hooded vultures (Nikolaus, We evaluated the potential impact of the traditional medi- ). Vultures have become rare, and their parts more expen- cine and commercial bushmeat trades on raptor populations sive, and therefore we expected that the contribution of black in West and Central Africa, based on counts of raptor car- kites to carcass counts might have increased over the years. casses offered for sale at market stands. We assessed the com- We estimated the numbers of raptors traded per annum, to position of raptor carcasses offered for sale, and investigated assess the potential impact of the regional trade on threatened the relationship between the numbers sold and morphologic- populations. al and ecological characteristics of the species identified. Our results were used to determine which species are most likely to be vulnerable to the trade and in which regions and coun- Methods tries. Based on previous studies we expected some taxa (e.g. vultures) and heavier-bodied species to be represented at Market inventories markets more frequently than other species (Nikolaus, ; Williams et al., ). We also predicted that a species’ migra- Carcass counts were conducted at fetish and bushmeat mar- tory status would influence its trade numbers. Afro– kets in the following countries throughout West and Central Palearctic migrants spend – months of the year at northern Africa (Fig. ): Benin, Burkina Faso, Cameroon, Democratic latitudes (with the exception of over-summering individuals Republic of the Congo, Equatorial Guinea, Gabon, Ghana, of some species) and were expected to be represented less Ivory Coast, Mali, Niger, Nigeria and Togo. These included commonly than Afrotropical resident species (i.e. those that our own counts conducted at intervals of one year or more are present year-round in the region), including intra-African during – in eight West African countries and three migrants. Controlling for species’ abundance, we expected Central African countries (Supplementary Table S). Our scavengers and savannah species to be recorded more fre- data were supplemented by published and unpublished re- quently than non-scavengers and forest species, which are as- ports of raptor carcasses recorded during surveys of bush- sumed to be harder to kill (i.e. poison) and detect, meat markets in Cameroon, Equatorial Guinea and Gabon respectively. As vultures are known to be an important during –. The latter counts were gathered from the

bushmeat database of the OFFTAKE project (OFFTAKE, vultures) were considered separately because they are particu- ), a collaborative project that collates datasets that larly highly valued by fetish traders and have undergone the quantify the offtake of terrestrial species (e.g. from subsist- greatest declines in the region (Thiollay, ). Black kites ence hunting, medicinal use, trophy hunting). Datasets for were considered separately because they are among the the OFFTAKE database were gathered by searching the lit- most common raptors in the fetish trade and are known to erature and contacting authors to request their raw data. be sold as substitutes for vultures. We also evaluated changes Our surveys covered mostly fetish markets in West Africa in the proportional contribution of black kites and hooded, and commercial bushmeat markets in Central Africa. palm-nut and large Afrotropical vultures among cumulative Stands were visited throughout the year, covering the nor- counts of raptor carcasses in all West African markets during thern winter and summer periods as well as the local dry –. Relative abundance of carcasses, rather than total and wet seasons (Supplementary Table S). Individual counts, was evaluated because survey effort and recorded stands were surveyed only once per year. A proportion of trade volumes varied between years. We used standard linear the same stands were revisited in different years, although regression to investigate whether the proportions of these relocation of stands and changes in ownership and stand raptors in counts varied between years. As necessary, data numbers made it difficult to track individual stands were log -transformed to meet the criteria of normality throughout the study period. For the same reason, the num- and homogeneity of variance. ber of stands visited each year varied (Supplementary Table S). Countries with larger, more numerous wildlife markets (e.g. Benin, Nigeria) were visited more often and Characteristics of traded raptors covered more extensively than countries where the trade was limited (e.g. Ghana, Togo). The markets surveyed Covariate modelling was used to evaluate predictions that were in villages and towns distributed over a wide geograph- total carcass counts for each species (i.e. the cumulative num- ical area and were approximately equally distributed among ber of complete skins or heads counted) increased with spe- forest (n =  locations) and savannah, and forest–savannah cies’ abundance and body mass, and varied according to main transition biomes (n = ; Fig. ), thus minimizing any site habitat, scavenging behaviour, phylogenetic position and mi- (i.e. habitat) effect on species composition of the overall gratory status. The abundance of each species was taken from sample. Some markets were visited more often than others, the most authoritative field guide for western Africa, from however, and the largest markets in Benin and Nigeria in Mauritania in the north-west to Congo in the south-east particular were located near or in the forest biome. In (i.e. overlapping with the study area and period of the some countries, such as Nigeria, only a proportion of well- study; Borrow & Demey, ). Species were categorized ac- known markets were visited, whereas most or all known cording to their abundance, as follows: scarce (encountered markets were visited in other West African countries. only irregularly, and infrequently to rarely within its normal Local interpreters assisted in locating markets and checking habitat), uncommon (encountered relatively frequently but stalls. Carcasses were enumerated by observing and count- not regularly within its normal habitat), not uncommon (usu- ing each raptor on display. Some birds were represented by ally, but not invariably, encountered within its normal habi- entire carcasses, others merely by their heads; both are re- tat), common (or locally common; invariably encountered ferred to here as representing a carcass. singly or in significant numbers within its normal habitat, sometimes only locally). Information on the main habitat (i.e. most commonly found (year-round): savannah, forest Trade per country and region or both), migratory status and mean body mass was also taken from the literature (Del Hoyo et al., ;Borrow& The proportion of hooded and palm-nut vultures Gypohierax Demey, ; Ferguson-Lees & Christie, ). Egyptian vul- angolensis, large-bodied (i.e. .  kg) Afrotropical vultures, ture Neophron percnopterus, peregrine falcon Falco peregrinus black kites and other diurnal raptors among total carcass and common kestrel Falco tinnunculus have Afrotropical and counts was calculated, to evaluate differences between coun- Palearctic breeding ranges and were considered Afro– tries (those with the largest markets: Nigeria, Benin) and re- Palearctic migrants based on the breeding range of the gions (West and Central Africa). We treated palm-nut and majority of individuals in West Africa (Thiollay, ). hooded vultures separately because they are both known to Because black kites were mostly yellow-billed kites (i.e. be commonly traded (Nikolaus, ); the first is a largely fru- the Afrotropical race aegyptius, which outnumbers the givorous, not uncommon vulture of wet savannahs and for- Palearctic race migrans in most of West and Central Africa, ests, and the second is a locally common scavenger of apart from in the far west), the species was considered an livestock carcasses, waste, faeces and other anthropogenic Afrotropical resident. Body mass was averaged for adult offal in and around settlements. Large Afrotropical vultures males and females. With regard to scavenging behaviour, (Rüppell’s, lappet-faced, white-backed, and white-headed species were categorized based on available information

TABLE 1 Explanatory variables used to examine the number of carcasses per species of raptors sold for fetish or bushmeat in markets in West and Central Africa (Fig. ) during –.

Covariate Description Abundance Common, not uncommon, uncommon, scarce Habitat Savannah, savannah & forest, forest Functional group A Non-scavenger, frequent scavenger, obligate scavenger Functional group B Non-scavenger, scavenger Functional group C Obligate scavenger, other Migratory status Afro–Palearctic migrant, Afrotropical resident Body mass Mean body mass (kg) of adults Phylogeny GYPINA Old World vultures (Aegypius, Gyps, Necrosyrtes, Torgos, Trigonoceps); ACCIPITRINA booted and hawk eagles, sparrowhawks, chanting goshawks, harriers, African fish eagle, black kite, buzzards, bat hawk (Aquila, Hieraaetus, Lophaetus, Polemaetus, Stephanoaetus, Accipiter, Melierax, Micronisus, Circus, Haliaeetus, Milvus, Buteo, Butastur, Kaupifalco, Macheiramphus); FALCONIDAE falcons (Falco); GYPAETINI Pernine kites, gymnogene, Old World vultures (Aviceda, Pernis, Polyboroides, Gypaetus, Neophron); CIRCAETINA snake eagles (Circaetus, Dryotriorchis); OTHER elanine kites, secretary bird, osprey (Elanus, Chelictinia, Sagittarius, Pandion)

on their diet composition in sub-Saharan Africa (e.g. Brown & obligate scavenger, () frequent scavenging (i.e. without dif- Amadon, ; Steyn, ; Mundy et al., ; Ferguson-Lees ferentiation between obligate and frequent scavengers), or &Christie,): non-scavenger (including species that scav- () obligate scavenging. Support for the latter would indicate enge only rarely or occasionally), frequent scavenger (sca- that obligate scavenging drives carcass abundance patterns, venges frequently but also consumes a significant whereas support for the second subdivision would suggest proportion of live prey; palm-nut and white-headed vultures, that abundance patterns were driven by frequent scavenging. tawny eagle Aquila rapax, black kite, Eurasian marsh harrier We used the corrected Akaike information criterion (AICc) Circus aeruginosus, bateleur Terathopius ecaudatus), and ob- value to select the most parsimonious models (those that fit ligate or near-obligate scavenger (Rüppell’s, lappet-faced, the data best with the fewest parameters; i.e. with the lowest white-backed, hooded, Egyptian vultures). Unlike other Old AICc; Burnham & Anderson, ), and the top four ΔAICc World vultures the white-headed vulture was not categorized of models as the cut-off criterion for delineating a set of top as an obligate scavenger because it is likely to consume live models. We computed model-averaged parameters by aver- prey regularly (Murn, ). The Eurasian marsh harrier fre- aging over all models in the set of top models. We used the quently scavenges in the European part of its winter range dredge function in R (part of the package MuMIn v. ..; (e.g. Hiraldo et al., ) and this is also likely to be the case Bartoń, ) to implement a model-averaging approach for in the Sahel (Zwarts et al., ). We used results of phylogen- the top models to make robust parameter estimates and pre- etic analyses based on nuclear and mitochondrial DNA to dictions (Johnson & Omland, ), and estimated the rela- classify raptor species into six groups (Lerner & Mindell, tive importance of each variable, based on the sum of Akaike ; Griffiths et al., ; Table ). weights. We subsequently evaluated the effect of variables We used generalized linear models with a negative bino- based on overlap of the % confidence intervals (following mial distribution and log link function using the package Burnham & Anderson, ). MASS in Rv.... (R Development Core Team, )to model how explanatory variables describing the various spe- Total numbers involved in the trade cies characteristics (Table ) affected total carcass counts per species, summed across all the data, including across years To determine the potential impact of the trade on raptor po- and across all sites. Habitat, functional group, phylogeny pulations, we estimated the number of raptors traded annu- and status were included as categorical variables, abundance ally at West African markets during –, using as an ordinal variable and body mass as a continuous vari- extrapolation of mean counts per market stand and able. We explored three sets of models, each consisting of known carcass turn-over rates. These estimates were based all possible subsets of combinations of explanatory variables, on carcass counts at  stands visited in ,  stands in including one of three explanatory variables for functional ,  stands in ,  stands in , and  stands in group (Table ). By including three subdivisions for the func- , in Benin, Nigeria, Mali and Burkina Faso. Because spe- tional group variable in each model set, we examined the rela- cies composition varied between Nigeria and Benin we cal- tive support for each of three alternative hypotheses: that culated mean counts per stand separately for these and the species carcass counts are best explained by ()anincreasing remaining countries, and extrapolated to the estimated total frequency of scavenging, from non-scavenger, to frequent, to number of stands. In Nigeria we visited approximately

one-third of the market stands trading in animal parts in , and therefore we tripled the number of stands to de- rive a country-wide estimate of  stands. We estimated a total of  stands for Benin and  for the remaining West African countries where surveys had been conducted. We cautiously estimated the minimum and maximum numbers traded based on turnover rates of two to three birds per stand per year, although detailed examinations for various species suggest that this turnover rate can be higher (– or more carcasses per year; Cocker, ; Nikolaus, ; Awoyemi, ; G. Nikolaus, unpubl. data).

FIG. 2 Percentages of black kites Milvus migrans, large Afrotropical vultures (Rüppell’s Gyps rueppellii, lappet-faced Results Torgos tracheliotos, white-backed Gyps africanus, and white-headed vultures Trigonoceps occipitalis), palm-nut Trade per country and region Gypohierax angolensis and hooded vultures Necrosyrtes monachus, and other raptors among raptor carcasses recorded at Black kite and hooded vulture together represented %ofa markets in Nigeria (n =  carcasses), Benin (n = ,), Mali,  total , raptor carcasses of  species recorded at markets Togo, Niger, Ivory Coast, Ghana and Burkina Faso (n = ), and Cameroon, Equatorial Guinea, Gabon and DRC (n = ) in West and Central Africa (Supplementary Table S). during –. Shikra Accipiter badius was the most commonly traded small raptor, comprising .% of the total carcass count. Afro– –   Palearctic migrants together represented .%ofcarcass during (linear regression: F, = . , β   ±        counts. This is assuming that short-toed Circaetus gallicus = . SE . ,P= . , adjusted R = . ). However, sur-  and Beaudouin’ssnakeeagleCircaetus beaudouini carcasses veys in may not have yielded a representative sample be- were divided equally between species, and excluding the cause a relatively small number of carcasses was recorded  – (likely) possibility that the Palearctic race migrans of black (n = )comparedtootheryears(n= ). Excluding  kite comprised a small proportion of black kite carcasses. from the analysis, a significant proportional increase of The most common Afro–Palearctic migrant among carcasses black kites over the years was apparent (linear regression:   β   ±        was the Eurasian marsh harrier. Palm-nut and Rüppell’swere F, = . , = . SE . ,P=. ,adjustedR = . ;  the most commonly recorded vultures, after the hooded vul- Fig. ), providing support for the idea that black kites have  ture. However, the contribution of vultures to total carcass been traded increasingly since the late s. No significant counts varied between countries and regions (Fig. ); whereas temporal trend was detected in the proportion of large   β −  ±     the greatest proportion and diversity of large Afrotropical vul- Afrotropical (F, = . , = . SE . ,P= . ,ad-  −  tures (Rüppell’s, white-backed, white-headed, lappet-faced vul- justed R = . ), palm-nut (linear regression on    β −  ±   tures) were recorded in Nigeria (%; n =  carcasses), log -transformed data: F, = . , = . SE . ,    −    relatively few were offered for sale elsewhere in West Africa P= . , adjusted R = . ) or hooded vultures (F, = . , β −  ±      −  (.%; n = ,). In Central Africa palm-nut vulture carcasses = . SE . ,P= . , adjusted R = . )among were recorded most commonly (%oftotalcounts;n= raptor carcasses. carcasses), contrary to the situation in West African countries –  ( % of carcasses). Overall, % of carcasses on offer were of Characteristics of traded raptors species categorized as threatened (Near Threatened to Endangered) on the IUCN Red List of Threatened Species Our models found strong support for an influence of spe- (IUCN, ). Of these (n = ), %werefoundinNigeria cies’ abundance, habitat, migratory status, and scavenging and % in Benin. Nigeria was the only country where the re- behaviour on carcass counts. All six plausible models (i.e. gionally threatened martial eagle Polemaetus bellicosus and sec- models with ΔAICc ,  of the top model; Table ) included retary bird Sagittarius serpentarius were recorded at markets the influence of species’ abundance and scavenging behav- (Supplementary Table S).Despitemorethanhalfofmarkets, iour, and five and four of the six top models featured habitat including some of the largest markets, being located in the for- and migratory status, respectively. Body mass was repre- est biome, % of carcasses were of species mainly associated sented once in the top model set, and phylogeny and func- with savannah habitats, suggesting that raptors are transported tional group C were not included. The four most important significant distances to commercial markets. predictors among the six plausible models, in decreasing The data did not indicate a significant increase in the pro- order of importance, were species’ abundance (relative im- portional contribution of black kites to total carcass counts portance: ), habitat (.), functional group B (.), and

–, white-backed vultures, –, lappet-faced vultures, and – crowned eagles Stephanoaetus coronatus. For –% of species (n = ) ,  individuals are estimated to be traded annually in West Africa.

Discussion

The diversity of raptor species, and number of individuals, offered at West and Central African markets, particularly in Nigeria and Benin, is considerable. Approximately %of the region’s diurnal raptor species were on sale, suggesting FIG. 3 Linear regression model of the relationship between the that many raptors are used as fetish species (Nikolaus, , percentage of black kites among raptor carcasses at markets in   West and Central Africa (Fig. ) and year of survey, during ; Williams et al., ) as well as bushmeat (Saidu & Buij,    –. ; Buij & Croes, ; Whytock et al., ). Our results indicate that Nigeria and Benin are import- status (.; Table ). The model-averaged parameters of the ant drivers of the regional trade in raptors in West Africa.  top models (Table ) strongly supported the hypothesis that This supports an earlier assertion by Nikolaus ( ) that more common species were represented more often among there is a high per capita use of raptors for fetish in carcasses than scarcer species. Forest species were less likely Nigeria and Benin. Fetish demand and prices of vultures  to be found in markets than savannah species, or habitat are particularly high in Nigeria (Nikolaus, ), where generalists that inhabit both savannah and forests (Fig. ). large Afrotropical vultures constituted a greater proportion Scavenging behaviour increased the probability of being of raptors traded compared to Benin or elsewhere in West traded compared to non-scavenging (Fig. ) but there was and Central Africa. Large Afrotropical vultures were already  little support for the idea that obligate scavenging alone largely extirpated in Nigeria in the early s (Nikolaus,  was responsible for this pattern (functional group C fea- ), and human-commensal hooded vultures have de-  tured only twice among models with AICc weights $ %; clined (Ogada & Buij, ). The diversity and number of Table ). Rather, our results strongly suggest that all species vultures for sale in Nigeria support anecdotal evidence that scavenge frequently (i.e. frequent and obligate scaven- and results of questionnaire surveys indicating that the gers) are traded more commonly than those that consume catchment area for Nigerian traders extends at least from   carrion only rarely or occasionally (Table ). Species with Burkina Faso to Chad (Nikolaus, ; Saidu & Buij, ). an Afrotropical breeding range were more likely to be traded Because large Afrotropical vultures or their eggs are valued ’ compared to those with a Palearctic breeding range (Fig. ). at several months salary, Nigerian poachers invest in ob- Although body mass featured in the top model set (relative taining them, sourcing them from countries in the wider re-  importance: .; Table ), the confidence intervals of the gion (Saidu & Buij, ). Shifts in pressure to other species, body mass predictor included zero, suggesting species’ such as migratory black kites, suggest that the trade has the body mass did not influence carcass counts. potential to affect raptor populations beyond West and Central Africa. For many West and Central African raptors the impact of Total numbers involved in trade the trade may be limited compared to other anthropogenic and climate-related factors that influence their food re- In West Africa during – an estimated ,–, sources, nest availability, and population dynamics (e.g. raptors were traded each year, based on extrapolated carcass Buij et al., a,b). The commercial trade, however, can be count data (Supplementary Table S). An estimated – implicated in the decline of vultures and other large raptors , raptors were traded each year in Benin, ,–, in the region. For some species, such as Rüppell’s, hooded, in Nigeria, and – in the rest of West Africa white-backed, white-headed, and lappet-faced vultures, the (Supplementary Table S). The bulk of the trade was in numbers traded probably represent a significant proportion Nigeria (% of carcasses), with % in Benin and % else- of their regional populations. Although rigorous population where in West Africa. Assuming turn-over rates of – indi- estimates are unavailable for most species, the extrapolated viduals per stand per year, an estimated ,–, hooded annual toll of lappet-faced vultures in West Africa during vultures and ,–, black kites were traded during the – represents as much as .–.%ofc., indivi- -year period in West Africa. Estimates for other commonly duals estimated to have occurred in West Africa and the traded large raptors during this period were ,–, Sahara during the s (Shimelis et al., ), assuming palm-nut vultures, ,–, Rüppell’s vultures, they were all sourced from this region. However, trade

TABLE 2 Top generalized linear models (Akaike weight . %) examining the relationship between cumulative carcass counts of  raptor species (Supplementary Table S;n=, carcasses) at markets in  countries in West and Central Africa during – (Fig. ) and the species’ abundance, habitat, functional group, phylogenetic position, body mass, and migratory status (Table ), with degrees of free- dom, corrected Akaike information criterion (AICc), ΔAICc and Akaike weight.

Model1 df AICc ΔAICc Akaike weight2 Abundance + habitat + functional group B + status 9 434.51 0.00 0.31 Abundance + habitat + functional group B 8 435.91 1.39 0.15 Abundance + functional group B + status 7 437.32 2.81 0.08 Abundance + habitat + functional group A + status 10 437.39 2.88 0.07 Abundance + habitat + functional group B + body mass + status 10 437.45 2.94 0.07 Abundance + habitat + functional group A 9 438.22 3.70 0.05 Abundance + habitat + functional group B + body mass 9 438.78 4.27 0.04 Abundance + functional group B + body mass + status 8 439.29 4.78 0.03 Abundance + functional group B 6 439.79 5.27 0.02 Abundance + habitat + functional group A + body mass + status 11 439.88 5.37 0.02 Abundance + functional group A + status 8 440.11 5.60 0.02 Abundance + habitat + functional group C + status 9 440.16 5.64 0.02 Abundance + habitat + functional group C 8 440.28 5.76 0.02 Abundance + habitat + functional group B + status + phylogeny 14 441.12 6.61 0.01 Abundance + habitat + functional group A + body mass 10 441.17 6.65 0.01 Abundance + habitat + functional group B + phylogeny 13 441.23 6.72 0.01 Abundance + functional group A + body mass + status 9 441.33 6.81 0.01 Abundance + habitat + body mass 8 442.00 7.49 0.01 Abundance + functional group A 7 442.33 7.82 0.01 Abundance + functional group B + body mass 7 442.36 7.84 0.01 Abundance + habitat + body mass + status 9 442.48 7.97 0.01 Abundance + habitat + status 8 442.68 8.17 0.01 Null 2 497.20 62.69 0.00

 Listed in order of most to least parsimonious model, after fitting combinations of all possible subsets with each of the three explanatory variables for functional group.  The weight of evidence in support of the model (cf. Burnham & Anderson, )

volumes may have constituted a higher proportion of popu- even with only a small decrease in adult survival rates lations remaining in –, as was the case for the white- (Whitfield et al., ; Oro et al., ;Ortegaetal.,). headed vulture. There were an estimated , or more Assuming the majority of vultures and other large raptors on white-headed vultures in West Africa in the s(Mundy offer at markets were killed specifically for trade, the trade et al., ), and .–.% of this number were channelled probably contributed to increased mortality rates and signifi- through the trade each year during –.Asthemost cant population declines, including the % decline of large recent estimate suggests that as few as  remained in  vultures outside protected areas in central West Africa during (C. Murn, unpubl. data), the annual trade constituted .–% – (Thiollay, ). of the remaining West African population. Hooded vultures, The percentage of vultures among raptor carcasses was which are under pressure from poachers, were estimated to highest in Central Africa, mostly accounted for by palm-nut number c. , individuals in West Africa (Ogada & vultures. The palm-nut vulture is an important and valuable Buij, ). Our estimates suggest that .–% of those were species for fetish purposes in West Africa, and individuals lost to the trade annually during –. Our estimates have been sold for c. USD  in Nigeria (Nikolaus, ). of annual tolls, even those based on more recent population We estimated its offtake in West Africa to be – indi- estimates, are likely to be biased low because we used conser- viduals per annum (i.e. .% of the continental population vative estimates of turnover rates to estimate numbers traded; of c. ,, most of which are in West and Central Africa; other studies suggest these may be significantly higher (e.g. Mundy et al., ). However, the true impact of hunting Awoyemi, ). Although we lack quantitative data, the ma- on palm-nut vulture populations may remain largely con- jority of raptors recorded at markets appeared to be adults, cealed, at least in Central Africa, where the vultures are which have a vital role in population dynamics, especially often consumed in bushmeat hunting camps rather than for larger species (Sæther & Bakke, ). Persecution may being transported to markets (Whytock et al., ). be one of the most important factors of non-natural mortality Although this highly prized species is categorized as Least in threatened populations of large raptors, which may decline Concern on the IUCN Red List (IUCN, ) because of

TABLE 3 Effects of species characteristics assumed to influence cumulative carcass counts of  raptor species (n = , carcasses) at markets in  countries in West and Central Africa during – (Fig. ), with model-averaged parameter estimates for each variable (Table ) in the six most strongly supported models (Table ), and the relative importance of explanatory variables.

Variable Parameter estimate (95% CI) Relative importance1 (Intercept) 3.59 (2.38–4.81) Abundance2 Not uncommon −1.35 (−2.11 – −0.60) 1.00 Uncommon −2.53 (−3.22 – −1.84) Scarce −3.50 (−4.69 – −2.31) Habitat3 Savannah 0.97 (0.21–1.73) 0.90 Savannah & forest 1.46 (0.59–2.32) Functional group B4 Scavenger 0.95 (0.38–1.52) 0.83 Status5 Afrotropical resident 0.66 (0.07–1.25) 0.72 Functional group A4 Frequent scavenger 0.80 (0.11–1.50) 0.17 Obligate scavenger 1.08 (0.32–1.84) Body mass −0.03 (−0.19–0.13) 0.10

 Calculated by summing Akaike weights across the top model set (Burnham & Anderson, ); % confidence intervals of the estimate not overlapping zero are indicated in bold.  Reference group: common  Reference group: forest  Reference group: non-scavenger  Reference group: Afro–Palearctic migrant

its large range, population size and apparently stable popu- particularly commonly traded, whereas trade in forest spe- lation, ongoing persecution warrants closer examination of cialists is comparatively uncommon. This relative scarcity its population trends. of forest-restricted species in the trade may be related to Other large raptors vulnerable to persecution include the difficulty in finding, shooting or poisoning these species, Africa’s largest eagles (martial and crowned). Extrapolation which are generally more elusive. The greater numbers of of the estimated annual toll suggests at least  crowned ea- Afrotropical residents in the trade, including intra-African gles were traded commercially in West Africa during – migrants, is probably related to their year-round availability; , which represents an unknown but probably significant the majority of Afro–Palearctic migrants spend much of the proportion of regional populations. Although these uncom- year outside the poachers’ catchment area. mon raptors are unlikely to be poisoned on a scale compar- Our models support the hypothesis that, together with able to scavengers, they may be shot; crowned eagles may be obligate scavenging vultures, raptors that scavenge frequent- lured by bushmeat hunters imitating the calls of prey animals ly are more likely to end up at markets compared to non- (Whytock & Morgan, ). This may occur more frequently scavenging species. We suspect this is related to the ease than previously thought, as crowned eagles were the second of killing most scavengers using poisoned baits, which is most common forest species and the commonest large rap- probably the most widespread method used to kill raptors tors (i.e. .  kg) recorded at markets after Rüppell’s, white- and other predator populations in sub-Saharan Africa backed and lappet-faced vultures. Their slow maturation rate (Ogada, ). Frequent use of human-dominated, low- and biennial reproduction in tropical forests make the quality habitats may increase the vulnerability to poisoning crowned eagle one of the most vulnerable raptors to direct of some obligate and frequent scavengers (black kite, persecution (Shultz, ; Whitfield et al., ), com- hooded vulture; Otieno et al., ; Kendall, ; Buij pounding negative impacts of habitat loss and degradation, et al., a). Some frequent scavengers (black kite, disturbance of nest sites, and prey depletion by bushmeat Eurasian marsh harrier) congregate at easily detectable hunters (Lindsey et al., ; Whytock et al., ). roosts, possibly increasing their vulnerability to poachers; The positive relationship between species’ abundance and the high search efficiency of others (bateleur, tawny eagle; carcass counts suggests that at a regional scale species are tar- Kendall, ; Kane et al., ) may facilitate poisoning geted indiscriminately to supply the trade. However, our re- or trapping using baits. Alternatively, some frequent scaven- sults showed that Afrotropical habitat generalists inhabiting gers may constitute bycatch of poachers targeting more forests and savannahs, and those of savannah habitats, are highly prized vultures.

FIG. 4 Plots of the modeled relationship between carcass counts of raptor species and the species’ (a) abundance, (b) habitat, (c) functional group B, and (d) status (Table ), as estimated by the top model (cf. Table ). Carcass counts are plotted on their original scale. The black horizontal line represents the model-predicted value, with all other variables set to their most common category, and the shaded areas indicate % confidence bands; the vertical ticks indicate number of observations.

It is possible that not all raptors recorded at markets therefore assume that the majority of raptors on offer at were killed for trade; casualties related to other anthropo- markets are probably killed deliberately for the trade, genic factors (e.g. electric power lines, roads, pesticides), or which is supported by information obtained from traders disease may also be sold in markets. However, indirect in Nigeria (Saidu & Buij, ). evidence suggests that mortalities related to these factors The trade in raptors for traditional medicine or for food is probably account for only a small proportion of raptors of- likely to have contributed considerably to the significant de- fered at markets. The electrical power transmission system cline of vultures and other large raptors, and possibly also to a over most areas in West and Central Africa is poorly de- number of smaller raptors, in West and Central Africa. veloped, unlike in North and southern Africa, where this is Within West Africa, Benin and Nigeria collectively accounted a significant cause of mortality (Nikolaus, ; Jenkins for % of the carcasses traded during –. et al., ). There are unlikely to be many raptor deaths Conservation efforts focused on these two countries would caused by road traffic given the condition of most roads therefore have the most significant impact on curtailing this prevents driving at high speed, which is confirmed by trade within the wider region. More than a quarter of raptors generally few raptor carcasses found along roads (R. Buij, sold at the markets surveyed in West and Central Africa since pers. obs.). Casualties from secondary pesticide poisoning  are categorized as threatened on the IUCN Red List also appear to be generally low, being significant only (IUCN, ), including five Afrotropical vultures that war- when colonies of red-billed quelea Quelea quelea are rant uplisting to Critically Endangered on the basis of popu- sprayed with fenthion when irruptions occur (Keith & lation decline (Ogada et al., ). A lack of population data Bruggers, ). Deaths of hooded vultures as a result of makes it difficult to conduct accurate Red List assessments for avian influenza may be significant, at least locally as some vulnerable species that are commonly exploited by the shown in Burkina Faso (Ducatez et al., ), but we are trade (palm-nut vulture, crowned eagle). Increasing prices are not aware of similar die-offs elsewhere in the region. We leading to increasing pressure on remaining vultures, as

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Oryx, , –. Biographical sketches OTIENO, P.O., LALAH, J.O., VIRANI, M., JONDIKO, I.O. & SCHRAMM, K.W. () Carbofuran and its toxic metabolites provide forensic R ALPH B UIJ studies relationships between land-use change, hunting, evidence for furadan exposure in vultures (Gyps africanus) in Kenya. and protected area management and population dynamics of birds and Bulletin of Environmental Contamination and Toxicology, , mammals in West and Central Africa. G ERHARD N IKOLAUS is an or- –. nithologist with many decades of experience in sub-Saharan Africa, RDEVELOPMENT CORE TEAM () R: A Language and Environment and the author of Distribution Atlas of Sudan’s Birds, with Notes on for Statistical Computing. R Foundation for Statistical Computing, Habitat and Status. He performed most of the market surveys Vienna, Austria. presented here. R OBIN W HYTOCK’s research interests include inves- RONDEAU,G.&THIOLLAY, J.M. () West African vulture decline. tigating the decline of Afro–Palearctic migrants, and the conservation Vulture News, , –. ecology of birds in the Lower and Upper Guinean forests. D ANIEL SÆTHER, B.E. & BAKKE,Ø.() Avian life history variation and I NGRAM is a conservation scientist and modeller investigating the ex- contribution of demographic traits to the population growth rate. ploitation of terrestrial species throughout the tropics. He is the man- Ecology, , –. ager of the OFFTAKE database. D ARCY O GADA is a conservation SAIDU,Y.&BUIJ,R.() Traditional medicine trade in vulture parts biologist whose main focus is East African raptors and combating poi- in northern Nigeria. Vulture News, , –. soning of wildlife.