Impacts of Disease on Vultures

This section looks at the impacts of the chemicals and diseases on individual species of vultures. Also examined are other factors for population declines, to discern the impact of chemical compounds and disease among other factors. The first group examined are the Eurasian vultures: Red-headed, Slender-billed, Indian, Griffon, Himalayan Griffon, Egyptian, Cinereous and Bearded vultures. The second group examined are the African vultures: Hooded, White-backed, White-headed, Ruppells's Griffon, Palm-nut, Cape and Lappet-faced vulture. After these, the last group are the New World vultures: Andean and California condors, King, Turkey, Greater Yellowheaded, Yellow-headed and Black vultures.

In general, the decline of the Eurasian vultures has been blamed on several factors: increased agricultural activities, the decline of wild ungulates, increasingly efficient sanitation, persecution and disease. The Red Headed vulture has been described as less affected by the drug diclofenac than other Asian vultures. This species may have avoided the worst effects, because of the dominance of the other larger species at the carcasses (Cuthbert et al. 2006) and the non-use of diclofenac in parts of its range, such as Myanmar (Eames 2007a) and Cambodia (Mahood 2012). In Cambodia, studies have shown that it is occasionally poisoned due to the use of such chemicals for catching fish and waterbirds at waterholes (ibid.).

The White-rumped, Slender-billed and Indian vultures were severely affected by diclofenac, especially in Nepal, Pakistan and India, dying from renal failure resulting in visceral gout (Oaks et al. 2004a; Shultz et al. 2004; Swan et al. 2005; Gilbert et al. 2006). Other causes were ketoprofen, which was also lethal (Naidoo et al. 2009), changes in the processing of dead livestock, non-target poisoning (Wildlife Trust of India 2009), avian malaria and pesticides (Poharkar et al. 2009).

The Red-headed vulture was already in decline in South-East Asia before the advent of diclofenac, the decline due to the serious decline of large wild ungulate populations, lower numbers of livestock, improved sanitation of livestock carcasses and use of poisons (Mahood 2012; Clements et al. 2013). For the Common Griffon, possibly because of the wider range, more factors are mentioned for its decline. These include poisoning and persecution (del Hoyo et al. 1994; Snow and Perrins 1998; Ferguson-Lees and Christie 2001), changes in livestock management practices (del Hoyo et al. 1994; Ferguson-Lees and Christie 2001) and wind energy development (Strix 2012).

For the Bearded vulture, the main causes of current declines are nontarget poisoning, direct persecution, habitat degradation, disturbance of breeding birds, inadequate food availability, changes in livestock-rearing practices and collisions with power-lines and wind farms (Ferguson-Lees and Christie 2001; Barov and Derhe 2011). Simmons and Jenkins (2007) note that population trends in southern Africa may be correlated with climate trends. Other threats include habitat degradation and breeding disturbance (Ferguson-Lees and Christie 2001).

For the Egyptian vulture, European problems include disturbances, lead poisoning (from shot animals), direct poisoning, electrocution (by powerlines), collisions with wind turbines, reduced food availability and habitat change (Donazar et al. 2002; Kurtev et al. 2008; Zuberogoitia et al. 2008; Carrete et al. 2009; Sara and Di Vittorio 2003; Sara et al. 2009; Dzhamirzoev and Bukreev 2009; BirdLife International 2014), and EU regulations from 2002, managing carcass disposal reduced food sources, especially by the closure of traditional 'muladares' in Spain and Portugal (Donazar 2004; Lemus et al. 2008; Donazar et al. 2009, 2010; Cortes-Avizanda et al. 2010; Cortes-Avizanda 2011).

New regulations permit the operation of feeding stations for scavengers (BirdLife International 2014). In Spain and the Balkans, the main threat is illegal poisoning for carnivores (Hernandez and Margalida 2009). Fatal levels of contamination also affect birds in Spain (Lemus et al. 2008) and Bulgaria (Angelov 2009). Antibiotic residues in the carcasses of intensively-farmed livestock also may increase diseases among nestlings (Lemus et al. 2008) (an example being avian pox in Bulgaria) (Kurtev et al. 2008). Diclofenac is another important factor, but possibly less for the Egyptian vulture than for the larger vultures due to competitive exclusion of smaller vultures from carcasses (Cuthbert et al. 2006). African threats for the Egyptian vulture include: the decline of wild ungulates and livestock overgrazing (Mundy et al. 1992); poisoning targeted at terrestrial predators (Carrete et al. 2007; Carrete et al. 2009; Cortes-Avizanda et al. 2009c); power line collisions, especially in the Canary Islands, other parts of Spain (Donazar et al. 2002; Donazar et al. 2007, 2010) and in Port Sudan (Nikolaus 1984, 2006); and killings for traditional medicine, e.g., in Morocco; and also competition for nest sites with Griffon vultures (Kurtev et al. 2008).

For the Cinereous vulture, problems include: accidental ingestion of poisoned baits for predator extermination; deliberate shooting and poisoning; and decreasing food sources. Shooting, poisoning and trapping occur in Mongolia and China (BirdLife International 2014). Diclofenac may increase due to wintering in northern India. Antibiotics such as quinolones damage the liver, kidneys, lymphoid organs and bacteria flora, increasing infections among vultures in central Spain (Lemus et al. 2008). Other problems are European Union legislation on carcass disposal, reductions of livestock in Georgia and Armenia, due to the cancellation of subsidies for sheep-herding in the post-Soviet era, wild ungulate decline (e.g., the Saiga antelope (Saiga tartarica Linnaeus, 1766), declining from over one million to 30,000-40,000 in ten years, due to excessive hunting and severe winters); food source declines in South Korea (Lee et al. 2006); and habitat loss and climatic instability, which kills nestlings (Batbayar et al. 2006).

For the African vultures, the Hooded vulture faces threats from nontarget poisoning, capture for traditional medicine and bushmeat, and direct persecution (Ogada and Buij 2011). Hooded vulture meat may be sold as chicken in some places. Poachers may also poison vultures to hide the locations of their kills. Carbofuran poisons in livestock baits intended for mammalian predators may also kill vultures in East Africa (Otieno et al. 2010). Other threats are land conversion through development and improvements to abattoir hygiene and rubbish disposal in some areas (Ogada and Buij 2011). The species may also be threatened by avian influenza (H5N1), which may also be acquired from discarded poultry carcasses (Ducatez et al. 2007).

For the White-backed vulture, threats are habitat conversion to agropastoral systems, declining populations of wild ungulates and less carrion, hunting for trade, persecution and poisoning (especially the highly toxic pesticide carbofuran) (Western et al. 2009; Ogada and Keesing 2010; Otieno et al. 2010). Diclofenac was also found on sale at a veterinary practice in Tanzania (BirdLife International 2014). Killings for medicinal and psychological benefits are also common in Nigeria and southern Africa (McKean and Botha 2007; Birdlife International 2014). These may lead to local extinction in some parts of southern Africa (McKean and Botha 2007). International trade in captured birds is also a problem, as is electrocution on powerlines and human disturbance in nesting trees (Bamford et al. 2009; BirdLife International 2014).

For the White-headed vulture, threats include reductions in wildlife, especially ungulates, and habitat conversion (Mundy et al. 1992; BirdLife International 2014). Some birds are poisoned by bait for jackals and larger carnivores such as lions and hyenas, and secondary poisoning from carbofuran (Otieno et al. 2010). The White-headed vulture is possibly less susceptible to these problems than other vultures as its diet is comparatively broader. It is also captured for the international trade in raptors and for traditional medicines in Southern Africa. Human disturbances may contribute to nest desertion. It is sensitive to land-use and hence concentrates in conservation areas (Hancock 2008b; BirdLife International 2014).

For the Ruppell's Griffon vulture, the threats are similar as it suffers from habitat conversion to agro-pastoral landcover, wild ungulate decline, persecution and poisoning and hunting for trade (Western et al. 2009; Ogada and Keesing 2010; Otieno et al. 2010). In West Africa it is exploited for trade in traditional medicines, possibly leading a decline and near extinction in Nigeria (Rondeau and Thiollay 2004; Nikolaus 2006). Examples are cited of the Dogon people of central Mali climbing the Hombori cliffs to take eggs and chicks of this species (Rondeau and Thiollay 2004). In Mali, breeding birds may be affected by the large numbers of tourists visiting climbing routes in the Hombori and Dyounde Massifis (Rondeau and Thiollay 2004).

For the Cape vulture, assumed to be declining throughout much of its range (Boshoff and Anderson 2007), threats include a decrease in the amount of carrion (particularly during chick-rearing), inadvertent poisoning, electrocution on pylons or collision with cables, loss of foraging habitat and unsustainable harvesting for traditional uses (Mundy et al. 1992; Barnes 2000; Benson 2000; Borello and Borello 2002; Diekmann and Strachan 2006; Boshoff and Anderson 2007; Hancock 2008; Boshoff et al. 2009; Jenkins 2010). Other lesser threats include disturbance at colonies, bush encroachment and drowning (Anderson 1999; Borello and Borello 2002; Bamford et al. 2007). In southern Africa, like other vulture species, Cape vultures are killed for perceived medicinal and psychological reasons (McKean and Botha 2007).

If the White-backed vulture declines or faces extinction as a result of these factors, the increase in hunting on Cape vultures could be devastating (Beilis and Esterhuizen 2005; McKean and Botha 2007). The reduction of a colony in eastern Botswana was blamed on human disturbance, including tourism (Borello and Borello 2002). Other problems are urbanisation around Hartbeespoort dam and the Magaliesberg mountains, South Africa, which has reduced natural food sources and increased reliance on vulture 'restaurants' (Piper et al. 1999; BirdLife International 2014). Bush encroachment into former grassland has also increased difficulties for foraging birds (Schutz 2007). Some birds in southern Africa drowned, possibly due to bathing or drinking attempts (Anderson et al. 1999; Boshoff et al. 2009). There are also fatalities due to powerline collisions and electrocutions, especially in Magaliesberg, South Africa (BirdLife International 2014). Climate also affects their habitats (Simmons and Jenkins 2007).

For the Lappet-faced vulture, declining populations are largely due to accidental poisoning, mostly from strychnine, which is used for predator control, and more recently carbofuran (Brown 1986; Komen 2009; Otieno et al. 2010; BirdLife International 2014). Some persecution is due to the belief that it kills livestock (Brown 1986; Simmons 1995). Other issues include reduced food availability, electrocution on power lines, agricultural pesticides, habitat loss, human nest predation and nest disturbance (Steyn 1982; Mundy et al. 1992; Shimelis et al. 2005; McCulloch 2006a,b). This species is especially sensitive to nest disturbance, with such a problem emerging due to forest settlement in Ethiopia (Steyn 1982; Bridgeford 2009; BirdLife International 2014).

Population reductions in West Africa have been blamed on ungulate extinctions through habitat modification and over-hunting, higher nest disturbance, intensified cattle farming without abandonment of dying animals and increases in accidental poisoning (Thiollay 2006a,b; Rondeau and Thiollay 2004). Available carcasses have been reduced, due to more effective livestock vaccinations and also the sale of carcasses to abattoirs rather than the disposal of such carcasses in rural areas. Hunting for medicine or food has also been suggested (Rondeau and Thiollay 2004). In Mozambique, the armed conflict in the 1970s and 1980s decimated wild ungulates and more recently the over-exploitation of game by poachers continues (Parker 2005b). Similar to other species, this species may be poisoned by animal poachers who believe that hovering vultures will expose their activities (Hancock 2009b).

For the New World vultures, the pattern is different. There is no drastic decline due to pesticides or other poisons. The larger species are rarer than the smaller species. The rarest was the California condor. For this species, threats that decimated the population during the 20th century were persecution, including shootings and lead poisoning from accidental ingestion of lead bullets and shot from carcasses (Parish 2012). Campaigns for condors appear to have reduced direct persecution (BirdLife International 2014). As already mentioned, lead poisoning is still a problem, after the reintroduction of captive birds into the wild, and several birds have died from poisoning (Cade 2007; Parish et al. 2007; Walters et al. 2010). The vulnerability of the condor also stems from its vast foraging range, in which any shot animals may be a risk factor and its slow breeding and long life, which allow a buildup of toxicity (Hunt et al. 2007).

Recent research has indicated that over 90% of released condors in Arizona are suffering from lead poisoning (Toops 2009). In January 2010 three birds died from lead poisoning in northern Arizona (Flagstaff 2010). In 2006, 9 of 13 birds released at the Pinnacles National Monument, California were recaptured for testing for lead poisoning, as they had eaten lead shot squirrels. Also in California, a study of samples from 2004-2009, found about one-third of condors had toxicological levels of lead from ammunition (Finkelstein et al. 2012). There are efforts to ban lead ammunition from areas within the species's range in California, and possibly there will one day be a ban on the use of lead across the United States.

Pesticide poisoning from DDT also affects the reintroduced condor population along the Central Pacific Californian coast, despite the lack of additional DDT inputs. The incidence of this poison may decline through time as more DDT is not being added to the environment. The result is reduced eggshell thickness causing problems with reproduction (Burnett et al. 2013). Possibly, the DDT is a derives from the carcasses of predatory marine mammals exposed to the DDT years previously (Burnett et al. 2013).

As also already mentioned, another threat to the California Condor is anthropogenic material, namely plastics and other manufactured products in the environment. For example, two nestlings died after swallowing plastic cartridge cases, glass fragments, wire, and other objects (Mee et al. 2007). Some hand-reared condors in the early 1990s died from collision with power-lines, necessitating a training programme using fake power poles to condition the birds to avoid the poles (Kiff 2005). Birds are also vaccinated against the possibility of the west Nile virus. The survival rate of the released birds is nevertheless unsustainable without treatment of lead-contaminated birds (Walters et al. 2010).

For the Andean Condor, the main threats are human persecution, partly based on the idea that condors attack wildlife (Houston 1994); and illegal poisoning of carcasses for the control of mountain lions and foxes (Imberti 2003). Changes in livestock rearing practices affect condors, which may be dependent on their carcasses (Lambertucci et al. 2009). There is also interspecific competition for carcasses with Black vultures (Carrete et al. 2009). For the King vulture, the main threat appears to be habitat destruction. For the Turkey vulture, the population is rather expanding, despite problems with lead poisoning as noted above. Populations of Turkey vultures are estimated to have increased by at least 100 percent over the last 40 years. The Black vulture has also expanded its range and population (BirdLife International 2014). For the Greater Yellow-headed vulture, the main issues are ongoing habitat destruction and over-hunting of prey species (del Hoyo et al. 1994; Ferguson-Lees and Christie 2001). For the Yellow-headed vulture, the population is described as stable (see chapter 3).