Arguably nature's most important scavengers, vultures provide essential ecosystem services by feeding on decomposing carcasses and thus reducing the risk of disease transmission (Ogada et al., Reference Ogada, Torchin, Kinnaird and Ezenwa2012). In India the collapse of vulture populations has resulted in an increase in the number of feral dogs, the main reservoir for rabies, which has subsequently led to an increase in rabies infections in humans; the associated health care cost is estimated to be USD 34 billion (Sudarshan et al., Reference Sudarshan, Madhusudana, Mahendra, Rao, Ashwath Narayana and Abdul Rahman2007; Markandya et al., Reference Markandya, Taylor, Longo, Murty, Murty and Dhavala2008). Despite their importance nearly 70% of vultures (and condors) are categorized as threatened or near threatened on the IUCN Red List (BirdLife International, 2015).
Populations of African vultures are at critically low levels. In just three generations the populations of seven species have declined by at least 80%, and four species have been recategorized as Critically Endangered and two as Endangered (Ogada et al., Reference Ogada, Shaw, Beyers, Buij, Murn and Thiollay2015; BirdLife International, 2015). Since the 1970s the major quantifiable threats to Africa's vultures have been poisoning (61% of recorded deaths) and unsustainable harvesting for trade in fetish (29%; Ogada et al., Reference Ogada, Shaw, Beyers, Buij, Murn and Thiollay2015). Across Africa poisoning is most often associated with illegal predator control, where lions Panthera leo, hyaenas Crocuta crocuta, leopards Panthera pardus, jackals Canis mesomelas and other predators are targeted by livestock farmers, and vultures typically become the unintended victims. Poison is the ultimate weapon as it is silent, cheap, easy and effective, and because of its illicit nature the majority of incidents are never detected or reported, making the true impacts on populations difficult to quantify (Vyas, Reference Vyas1999; Ogada, Reference Ogada2014).
Beginning in 2012 a substantial new threat to Africa's vultures emerged as a consequence of a spate of elephant poisonings linked to ivory poaching. Prior to 2012 there were a few, mostly anecdotal reports linking vulture mortality to elephant poisoning (Ledger, Reference Ledger1980; Truscott, Reference Truscott2011; Roxburgh & McDougall, Reference Roxburgh and McDougall2012), which indicates that the threat probably began earlier but remained poorly documented and underreported. During 2012–2014 mortalities associated with elephant poisoning accounted for one-third of all vulture mortalities recorded since 1970 (Ogada et al., Reference Ogada, Shaw, Beyers, Buij, Murn and Thiollay2015). Typically vultures were poisoned in large numbers while feeding on contaminated elephant carcasses, the most commonly reported species being the white-backed vulture Gyps africanus, followed by the lappet-faced vulture Torgos tracheliotos. However, in the majority of incidents the species of vulture was not determined, either because the observer was inexperienced or the carcasses were in an advanced state of decay. For these reasons no information on age class has been reported. Hooded Necrosyrtes monachus, white-headed Trigonoceps occipitalis and Cape vultures Gyps coprotheres have also been recorded but the latter two are frequently misidentified as white-backed vultures by field-based personnel who often report on these incidents but have limited bird identification skills. In addition to vultures, other scavenging species are killed at poisoned elephant carcasses, including hyaenas and bateleurs Terathopius ecaudatus.
During March 2012–July 2014 there were 11 known incidents in which vultures were poisoned at the carcasses of elephants that had been killed illegally, in seven sub-Saharan African countries (Table 1). One hundred and thirty-five of the 155 elephants killed were poisoned in a single incident in Zimbabwe, where cyanide was used. Collectively, the 11 incidents caused the deaths of at least 2,044 vultures (mean = 186 vultures per incident; range 1–500) as well as one lion, five hyaenas, two African wild dogs Lycaon pictus and two bateleurs, illustrating the disproportionate vulture mortality associated with ivory poaching. Although the majority of incidents reported here occurred in southern Africa, we have heard of at least two unsubstantiated cases from East Africa.
Table 1 Details of 11 vulture poisoning incidents at elephant carcasses poached for ivory in seven African countries.
* Estimates based on the number of vulture skulls and other bones found at the scene.
The rate of increase in vulture mortality as a result of poisoning associated with ivory poaching since 2012 greatly exceeds that associated with other types of poisoning incidents since 1970 (Fig. 1). Similarly, the number of vulture fatalities associated with each ivory poaching incident (median = 191; n = 11) is more than 30 times that recorded in other poisoning incidents since 2012 (median = 6; n = 33). Since 2014 ivory poaching incidents leading to multiple vulture fatalities have continued to occur, most recently in northern Kruger National Park, in September 2015 (A. Botha, pers. obs.), and in a series of incidents in Hwange and Matusadona National Parks, Zimbabwe, in October 2015 (News24, 2015). We emphasize again that underreporting and the illicit nature of poisoning incidents mean that the number of fatalities reported here is probably an underestimate. Although it may appear that vultures are merely unintended victims in these incidents, poachers have a strong motive to kill vultures, whose overhead circling is an indicator of a dead animal lying below. Because vultures inadvertently perform the role of aerial sentinels, revealing the poachers’ locations to local wildlife authorities, they have become targets in their own right (Roxburgh & McDougall, Reference Roxburgh and McDougall2012; Groom et al., Reference Groom, Gandiwa, Gandiwa and van der Westhuizen2013; Ogada, Reference Ogada2014). In at least two incidents, in Zimbabwe (Groom et al., Reference Groom, Gandiwa, Gandiwa and van der Westhuizen2013) and in South Africa (A. Botha, unpubl. data; Table 1), the poachers had an additional motive, to kill vultures for their body parts (typically the head), which are used for fetish.
Fig. 1 Cumulative African vulture deaths caused by illegal poisoning (n = 6,011), associated either with ivory poaching (n = 2,044), in which vultures are targeted, or with other poisoning incidents (n = 3,967), in which vulture deaths are typically incidental.
Worryingly, there is evidence that the use of poisons to kill elephants and rhinoceros in sub-Saharan Africa is increasing. The first known report of rhinoceros poisoning in South Africa was in 2005 (Reuters, 2005), and the intensive and widely reported use of poisons to kill elephants elsewhere in sub-Saharan Africa began in 2012. A total of six rhinoceros and 181 elephants are known to have been poisoned in 17 incidents in Botswana, Democratic Republic of Congo, Mozambique, Namibia, South Africa, Tanzania, Zambia and Zimbabwe (Table 1; Reuters, 2005; The East African, 2012; Guardian, 2012; Moonga, Reference Moonga2013; Endangered Wildlife Trust, unpubl. data). These numbers are probably underestimates of the actual totals, given both underreporting and the difficulty of obtaining mortality data related to poisoning of elephants and rhinoceros. Recent killing methods include lacing watermelons, oranges and pumpkins (and cabbages in the case of rhinoceros) with pesticides (e.g. aldicarb and carbofuran), and poisoning salt licks and waterholes with pesticides or cyanide. All of these methods kill non-target species and are environmentally destructive; however, the tainting of waterholes is particularly reckless given the myriad species that rely on them, including humans and livestock.
The recent surge in the use of poisons for poaching represents a further exploitation of weak regulations and enforcement regarding the accessibility and misuse of toxic pesticides and other substances. As a first step, African governments must ensure that pesticides listed on Annex III of the Rotterdam Convention (2015) and others that are widely implicated in wildlife poisoning (e.g. carbofuran) are no longer freely available over the counter, restricting their sale through a small number of licensed and trained distributors, and sold only in limited quantities to individual customers. Distributors should maintain a registry of the names and contact information of customers, and of the quantities of these pesticides sold, so that their misuse can be tracked more easily. Illegal importation or smuggling of these substances should also be stamped out at ports of entry.
International donors supporting anti-poaching efforts need to recognize the seriousness of this threat, and work with their African partners to curtail it. Industries involved in the manufacture or use of the most abused poisons (aldicarb, carbofuran and cyanide) must take greater responsibility for their misuse, and develop innovative solutions to phase out their manufacture and use. We further recommend: (1) Strengthening the legal framework to prosecute offenders and their employers; (2) Improving laboratory testing facilities in order to prosecute offenders; (3) Education regarding pesticide regulations, including training of law enforcement officers, sensitizing of magistrates, and national campaigns to raise awareness; (4) Training rangers and other field personnel to manage incidents effectively, including neutralizing poisoning sites, and collecting reliable data on incidents so that preventative actions can be focused; (5) Establishing a single continent-wide database to monitor the scale and distribution of poisoning incidents, and requiring national wildlife authorities to submit all poisoning data regularly; (6) Investigating the effects on human health of ingesting meat or of using vulture body parts harvested from poisoned carcasses.
Unrestricted access to toxic pesticides and poisons is having devastating effects on Africa's natural resources and the people who rely on them. As billions of dollars are being spent on the war against poaching, poachers are adopting increasingly secretive and lethal means of killing pachyderms, with devastating consequences for vultures. Wildlife authorities in many African nations are overwhelmed by the increasing use of poisons for poaching (Guardian, 2012; Moonga, Reference Moonga2013). This includes their use in the widespread harvesting of bushmeat and fish, with unknown consequences for human health (du Feu, Reference du Feu2001; Opare-Ankrah, Reference Opare-Ankrah2007; Odino, Reference Odino and Richards2011; Mzumara et al., Reference Mzumara, Perrin and Downs2015).
Whether these illicit activities will prove responsive to the measures advocated here remains to be seen, given that the recent acceleration in vulture poisoning is the work of elephant poachers, for whom the implementation of trade controls is likely to be of little consequence as they are already operating outside any legal framework. However, we should recognize that the intensity with which poisons are now being used to kill elephants, rhinoceros, vultures and, incidentally, other species, represents a paradigm shift. African governments should be afforded the international legislative backing and material support required to apply more punitive sentencing in cases of poaching with poisons.
Acknowledgements
We thank M. Kinnaird and C. Beale for helpful comments, and P. Hancock and J. Bradley for reports from Botswana. We also thank T. Otto and R. McRobb for reports from Mozambique and Zambia, respectively. J. Blanc provided comments and further information regarding elephants. We particularly thank the reviewers, A. Margalida and P. Mundy, whose helpful comments improved the manuscript.
Biographical sketches
Darcy Ogada is a conservation biologist whose main focus is East African raptors and combating wildlife poisoning. André Botha manages the Birds of Prey Programme of the Endangered Wildlife Trust, South Africa, and is also the Co-chair of the Vulture Specialist Group of the IUCN Species Survival Commission. Phil Shaw's research is focused on bird conservation and on the contrasting life histories of temperate and tropical birds.
