Poisons and other Diseases that Affect Vultures

Vultures are highly vulnerable to a range of threats, largely due to their specialized lifestyles. Avian specialization has been described as a possible factor for increased extinction risk (Sekercioglu et al. 2004). 'Avian scavengers have the highest percentage of extinction-prone species among avian functional groups' (Ogada et al. 2012: 453; see also Sekercioglu et al. 2004). Vulture declines are blamed on poisoning (Pain et al. 2003; Hernandez and Margalida 2008), food scarcity, hunting, and land-use changes (Rondeau and Thiollay 2004). Vultures are biologically specialized to deal with certain pathogens, as their stomach acids can detoxify bacterial toxins such as anthrax, reducing the risk of disease spread (Houston and Cooper 1975).

One important problem is ingestion of artificial products, such as plastic products (termed junk) discarded in the environment, which may be mistaken by vultures for bone fragments. When swallowed, such items may cause 'choking, poisoning, intestinal obstruction, malnutrition and death' (BirdLife International 2008c). Research shows that vultures and condors actively scavenge for bone fragments for both calcium needs and food pellet regurgitation, a habit that can influence them to swallow undesirable items that may harm them. Nestlings are at greater risk because they cannot regurgitate the indigestible objects, and may thus be subjected to choking, poisoning, intestinal obstruction and malnutrition (Ferro 2000). For example, for the reintroduced California condor, 'junk-induced nestling mortality is seriously threatening the re-establishment' of this species. One study found up to 650 junk items in nests, including glass, metal and plastics (Mee et al. 2007).

This is similar to the lead poisoning that brought the species to near extinction before 1987 (Cade 2007). Records indicate that six of the eight nestlings that either died in the nest or where taken from the wild since 2002 had swallowed pieces of plastic piping, cloth and rubber, and also glass, metal bottle-tops and even ammunition cartridges. Impacts on the nestlings included zinc poisoning, retarded feather development resulting from malnutrition (this caused by distended and blocked digestive passages), and in some cases, death (Mee et al. 2007). An important factor is the increased level of such discards in the environment since the reintroduction of the California condor, usually near urban areas (Mee et al. 2007).

For other vulture species, examples are the nests of the White-rumped vulture in Pakistan which frequently contain bits of china, metal and glass, possibly swallowed by nestlings. Nestling mortality from swallowing metal objects has also been cited as a factor behind the low breeding success of Griffon vultures in Israel and Armenia (Ferro 2000; Houston et al. 2007; BirdLife International 2008).

Lead poisoning from bullets in carcasses is dangerous to vultures (Garria-Fernandez et al. 2005; Cade 2007; Dobrowolska and Melosik 2008; Gangoso et al. 2009). Mateo-Tomas and Olea (2010) note that hunting may also have negative effects; with lead poisoning being the most important. Therefore, it is recommended that the ingestion of lead is monitored for deleterious effects (Patte and Hennes 1983; Pain and Amiard-Triquet 1993; Miller et al. 2000).

Turkey vultures (Cathartes aura) show marked individual variation in lead poisoning. Symptoms of lead poisoning include weakness and lack of coordination. High levels may result in lead toxicosis (Carpenter et al. 2003).

One study of hunting and its impacts on Turkey vultures in California, noted that although lead ammunition has been banned from waterfowl hunting in North America for nearly 20 years, lead ammunition is still widely used for big and small game animal hunting (Kelly and Johnson 2011). The lead exposure in turkey vultures was found to be significantly higher during the deer hunting season compared to the off-season. The lead exposure of the vultures was also positively correlated with increased intensity of wild pig hunting.

Lead-related mortality was a factor for the decline of the California condor population during the 1980s. This also affected the precarious, reintroduced wild population, and some condors required medical attention (Snyder and Snyder 2000; Kelly and Johnson 2011). Several studies have found high levels of lead in the blood of condors (Pattee et al. 1990; Hall et al. 2007; Hunt et al. 2007; Sorensen et al. 2007), although the high blood concentrations have also been found in condors outside the hunting season (Pattee et al. 1990). The impact on condors and the fact that the condor is an endangered, highly observed species resulted in major actions that culminated in the ban on the use of lead ammunition 2008 for most hunting activities in the condor's California range. There was also input from groups desirous of similar bans to protect other species and those who question the links between lead exposure in wildlife and hunting activities. Higher blood levels of lead were also found in other species, such as golden eagles within the condor's range (Pattee et al. 1990) and in ravens in the Greater Yellowstone Area, the latter especially during the big game hunting season (Craighead et al. 2009).

The poisoning of Turkey vultures through lead has also been reported in Canada (Clark and Scheuhammer 2003; Martin et al. 2008). In the former study, 184 individual raptors from 16 species were found dead across Canada. One Turkey vulture had 'highly elevated bone-lead concentration' (Clark and Scheuhammer 2003: 23). Other affected species included Red-tailed hawks, Great horned owls, and Golden eagles (131 of the 184 specimens) and 3 to 4% of the deaths were attributed to lead poisoning. The evidence pointed to dietary reliance on game birds and mammals killed by lead projectiles from ammunition used in upland hunting. In the study by Martin et al. (2008), 225 individual dead birds from 19 species of terrestrial raptors in southern Ontario were dissected for analysis of bone, kidney and liver tissues. Turkey vultures were found to have the 'highest mean concentrations of lead in bone and kidney compared to other raptor species'; although only one bird was found to have lead levels described as acute. There were also levels above the subclinal level in four others (Martin et al. 2008: 96). The continued use of lead shot for upland hunting is a primary source of lead and a continued risk to the raptors and scavengers.

Old World vultures are also affected. In a Spanish study, vultures were found to be strongly affected by spent lead ammunition in carcasses (Rodriguez-Ramos et al. 2009: 235). 'This exposure may have increased after the ban on abandoning carcasses of domestic ruminants in the field due to the bovine spongiform encephalitis (BSE) crisis, both because the vultures consume hunting bag residues more frequently and because malnutrition may lead to mobilisation of lead stores' (Rodriguez-Ramos et al. 2009: 235; see also Inigo and Atienza 2007). There is little information on the potential correlation of blood lead levels and clinical signs and potential subclinical effects of lead in vultures despite the evidence of clinical intoxication in Griffon vultures (Gyps fulvus) and Cinereous vultures, and other species (Mateo et al. 1997; Mateo et al. 2003; Hernandez and Margalida 2008). Rodriguez-Ramos et al. (2009) conclude that the high blood lead levels were derived only from the ingestion of spent lead ammunition (see also Garcia-Fernandez et al. 2005). The clinical symptoms of the lead toxicosis included disorientation, ataxia and impaired landing, posterior paresis, and severe hypochromic anemia. The higher lead levels were in birds admitted to the rehabilitation centers from mid-August to mid-February; correlated with the game hunting seasons.

In a study by Donazar et al. (2008: 89) on Egyptian vultures in the Canary Islands, blood samples showed high frequencies of lead poisoning; sub-clinical and clinical intoxication levels; 'these were probably caused by the ingestion of lead shot' (ibid.). The study found that 16% of birds had >0.2 ppm of Pb, these levels were high enough to cause declines in productivity (Ochiai et al. 1992; Burger 1995), physiological injuries and possibly death. Although the lead may be derived from scavenging on bird carcasses containing lead, in some cases some of the lead shot are rejected within pellets, but this is difficult to detect without a radiological study of the pellets (see Medina 1999, for another study of Egyptian vultures and Mateo 1998). It is suggested that lead pellets should be replaced by bullets of steel or molybdenum/tungsten alloys for hunting.

Another example was of vultures interacting with illegal elephant hunters in Namibia (Salisbury 2013). Illegal poaching of African elephants and White and Black rhinoceroses has increased, and carcasses are poisoned to kill vultures, because the large flocks of attendant vultures reveal carcass locations. In a recent (2013) incident, 600 vultures are reported to have died when they fed on a poisoned elephant carcass near Namibia's Bwabwata National Park. Salisbury (2013) quotes Leo Niskanen, Technical Coordinator, IUCN Conservation Areas and Species Diversity Programme; 'By poisoning carcasses, poachers hope to eradicate vultures from an area where they operate and thereby escape detection. The fact that incidents such as these can be linked to the rampant poaching of elephants in Africa is a serious concern. Similar incidents have been recorded in Tanzania, Mozambique, Zimbabwe, Botswana and Zambia in recent years' (ibid.). In the cited incident, the vultures were incinerated before detailed study, so the details were not conclusive. However, for two of the birds, the tags indicated that the birds originated from Kimberley in South Africa, about 1000 km distant from the place of their death.

Pesticide poisoning is another danger for vultures. For example, Hernandez and Margalida (2008), found incidents of pesticide poisoning of the Cinereous vulture (Aegypius monachus) in Spain during the period 1990-2006. Two hundred and forty one incidents related to 464 vultures were investigated. The possible classifications of the pesticide use were: approved use, misuse, or deliberate abuse. The method of application, spatial and temporal variation and reasons for the pesticide abuse were also investigated. Up to 98% of the incidents were intentional poisoning. Approved use was responsible for only a minor fraction (1.3%). Pesticide mortality affected vultures (83%). Three chemical compounds carbofuran, aldicarb, and strychnine, accounted for up to 88% of the cases, but eight others were also used. The illegal control of predators was the main factor for application. The Cinereous vultures were not seriously threatened, but the availability of highly toxic pesticides could increase illegal usage with more serious effects. The authors suggest that the elimination of the few frequently used compounds would benefit vultures and other wildlife without seriously affecting agriculture.

Agricultural pesticide poisoning is also serious in South East Asia. A study by Clements et al. (2012) found that vulture populations in Southeast Asia declined before the calamitous diclofenac episode in South Asia (Pakistan, India and Nepal). Common SE Asian vultures were the White- rumped, Slender-billed and Red-headed vultures, which ranged from southern China southwards into Myanmar, Thailand, and Peninsular Malaysia (Pain et al. 2003). By the 1980s, however, these species were either depleted or extirpated from southern China, Thailand and Malaysia (Round and Chantrasmi 1985; Round 1988; Zheng Guangmei and Wang Qishan 1998; Wells 1999). After the end of military conflicts in Cambodia, Lao People's Democratic Republic (PDR) and Vietnam, the vultures were restricted to areas bordering Cambodia in Lao PDR and Vietnam (Barzen 1995; Desai and Lic Vuthy 1996; Le Xuan Canh et al. 1997; Brickle et al. 1998; Timmins and Men 1998; Thewlis et al. 1998; Goes 1999; Long et al. 2000; Timmins and Ou 2001; Eames et al. 2004). It is speculated that the decline in vulture populations was due to the decline in numbers of wild ungulates, changes in husbandry of domestic stock and direct persecution.

The three species (White-rumped, Slender-billed and Red-headed vultures) were found only in Myanmar (Hla et al. 2011) and northern and eastern Cambodia by the 2000s (Hla et al. 2011), despite evidence that they had not been affected by diclofenac. Clements et al. (2012) argue that as these Cambodian birds represent one of the few populations of the three species outside South Asia where diclofenac was not used, their conservation is crucial. The populations of each of the three species are estimated at 50-200+ individuals.

Mortality was inferred to be the result of accidental poisoning, from strychnine or organophosphates from hunting and fishing (73%) normally used in agriculture and hunting or capture for traditional Khmer medicine (15%) (Timmins et al. 2003). Most poisoning incidents were intended to kill scavenging species (e.g., storks) and frugivores (fruit-eating animals), and also feral dogs, but vultures became the unintended victims (Cheke 1972). Killings using guns also occurred, as in the 1970s-1990s, during and just after the Kampuchean and Vietnamese wars, firearms were common (Wille 2006). However, the number of guns declined from the late 1990s (EU ASAC 2009). Some vultures also were affected by the HPAI H5N1 virus and at least one bird died of this ailment, but a survey found that some vultures carry antibodies to the avian encephalomyelitis virus (a picornavirus causing neural deficits in young poultry) (Gerlach 1994; Clements et al. 2012).

Deliberate and accidental poisoning contribute to the decline of Hooded vultures in Africa (Ogada and Buij 2011). Steep declines have been recorded in Cameroon, Uganda and Kenya and Southern Africa, largely through poisoning (Zimmerman et al. 1996; Mundy 1997; Thiollay 2001; Ogada et al. 2010; Ssemmanda and Pomeroy 2010; Virani et al. 2011). Poachers poison vultures in Botswana, in the belief that the vultures will reveal their illegal kills (Hancock 2009a, 2010). In Namibia, vultures are principally killed by poisons intended for problem mammals such as lions, hyenas and jackals (Bridgeford 2004). This also true of other parts of southern Africa (Anderson 1999; Verdoorn et al. 2004; Roche 2006). Pain et al. (2003) also report deliberate poisoning in southern Africa. Poisoning campaigns were intended to eliminate scavenging birds and eagles from the farming areas in Namibia in the 1980s. Where there was no poisoning in the nearby national parks of Kalahari Gemsbok and Etosha, the species remained at the previous levels (Mundy et al. 1992).

In another study in South Africa, van Wyk et al. (2001: 243) examined 'whole blood, clotted blood, heart, kidney, liver and muscle samples' from White-backed, Cape and Lappet-faced vultures and found 'the presence of quantifiable residues of 14 persistent chlorinated hydrocarbon pollutants.' They also compared the pesticide levels between nestlings from natural breeding colonies, adults from a wildlife area and also captive birds. The researchers found statistically significant differences between these populations with lower amounts for the captive birds for certain chemicals in pesticides: gamma-BHC (lindane), alpha(cis)-chlordane and alpha- endosulfan. The researchers acknowledged that the 'respective biocides measured in vulture samples were generally low in comparison to results documented for a number of avian species' and 'although no threat is posed by any of the organochloride pesticides' there should be continuous monitoring of breeding colonies and White-backed vulture nestlings may be used as bioindicators (ibid. 243).

Among the New World vultures, disease rarely contributes to serious declines in population. Kiff (2000) reports that populations of Turkey and Black vultures are even spreading northwards from the United States into Canada. Snyder and Snyder (1991) note that Turkey vultures are resistant to some natural pathogens, and even some rodenticides such as the compound 1080 (Sodium fluoroacetate). However, other poisons, such as cyanide and strychnine, which were formerly used to poison coyotes and any other predators of cattle and sheep, are serious threats to the vultures. Wilbur (1978), Kiff et al. (1983) and Coleman and Fraser (1989) report that DDE (dichlorodiphenyldichloroethylene) induced eggshell thinning. Wilbur's report noted 11%, 12% and 18% thinning of eggshells in post DDT (1947) California, Florida and Texas, respectively. Kiff et al. (1983) found thinning of 9.7%, 15.9% and 10.1% in the same states. Coleman and Fraser (1989) also found thinning among Turkey vulture eggs in southeastern and mid- Atlantic states during the period 1947-1964. Kiff (2000) notes that there is no evidence that DDT (dichlorodiphenyltrichloroethaneuse) hampered later expansion of vultures towards the northern United States, despite some evident population reductions in the southern states.