Vultures, Agricultural Development and Rural Environmental Change

Vultures have had a long interaction with people engaged in agriculture and other rural activities, either as perpetrators of disease, predators of small livestock or in a more positive light, as removers of carrion. Mateo-Tomas and Olea (2010: 520) refer to the 'huge dependence of vulture populations on farming activity' (see also Mum and Anderson 2008). Recently, human applied chemicals have also become important (Pain et al. 2003; Green et al. 2006), as have sanitary restrictions based on bovine spongiform encephalopathy in cattle, which affected vultures in Europe (Tella 2001; Camina and MonteHo 2006), antibiotics in livestock that affect vultures in Spain (Lemus et al. 2008) and attacks by Black vultures on cattle in the United States (Avery and Cummings 2004).

These issues applied to both the New World and Old World vultures. A major effect of agriculture and also urbanization, which may affect vultures is deforestation and either savannaization or in extreme cases, desertification as was described in Part 2. Savanna is an important foraging area for vultures. As noted in Chapter 3, in the Americas, the Yellow-headed Vulture has been called the savanna vulture, and with the exception of the other Cathartes vultures which have a sense of smell, all other vultures find food more easily in the open terrain, or like the King vulture they may follow Cathartes vultures to the carcasses in dense vegetation. In Africa and Asia, vultures forage principally in open terrain, mostly savanna. In West Africa, the small Hooded vulture is the main species found in the forest, while the larger vultures are principally denizens of the savanna. In Asia, open or mountainous terrain is the main vulture habitat. This section looks at the main interactions between vultures and rural people in terms of agriculture and food access change, as the other main environmental issues were discussed in Part 2.

Interactions between agriculturists and vultures concern not only the impacts of people on vultures, but also the impacts of vultures on human activities. The main issues concern the extent to which vultures may make use of the activities and products of farming and livetstock rearing for food access. Concerning crops, the main issue is environmental change, as most vultures (with the exception of the Palm-nut Vulture) are not fruit eaters. Open farmland may also attract herbivorous animals and ploughed soils may expose small animals that may attract vultures. Livestock rearing is generally more important, as vultures may feed on the caracsses of dead livestock such as cattle, and may even kill small or young livestock.

Kirk and Gosler (1994) studied migratory and resident Turkey and Black vultures in the Llanos of central Venezuela. The resident Turkey vultures were the smaller subspecies (Cathartes aura ruficollis) and the migrants were the Northern subspecies Cathartes aura meridionalis (that is in Venezuela for the northern Boreal winter, which approximately coincides with the dry season of northern South America, between October and April). The Turkey and Black vultures focussed mostly on different types of carcasses (Stewart 1978; Coleman and Fraser 1987). Turkey vultures favored carcasses of small mammals, while Black vultures favored mostly domestic livestock, which was 'a more predictable and abundant food source' (ibid. 940).

The smaller resident Turkey vultures foraged over forest, where the larger migrant Turkey vultures were rare, rather than savanna, where the migrants were common. The biomass of carcasses, especially of domestic livestock (which were restricted to the savanna) was higher in the savanna than in the forest. Migrants, being larger won almost all conflicts with residents over carcasses (470 to 1 of the conflicts observed). The unequal competition between the migrants and residents affected the health of the latter, as the study found that the condition of resident Turkey vultures was below average when they lived with migrants, and in above-average condition when the migrants were absent. The residents began to forage again in the savanna when the migrants moved northwards.

In northern North America, public attitudes towards the Black vultures has been partly shaped by the belief that the vultures affect farm animals. Kiff (2000: 180) noted that 'throughout the first half of the present century, many ranchers and farmers associated turkey and black vultures with the spread of diseases, especially anthrax, and therefore often sought to eliminate them, usually by trapping.' Black vultures were also believed to attack newborn calves. As a result, both Turkey and Black vultures were persecuted, using both private and government sponsored programs. These killed hundreds of thousands of birds in Florida and Texas during the 1940s and 1950s, before the later protection of both species by the Migratory Bird Treaty Act, signed by the United States, Canada and Mexico (Howell 1928; Parmalee 1954; Snyder and Rea 1998; Kiff 2000). In some areas, with large roosting centers, attempts have been made to disperse the birds on the premise of public nuisance 'generally by non-lethal means', but such measures are increasingly rare due to greater tolerance of wildlife in the USA over the years (Kiff 2000: 180).

The National Wildlife Research Center's (NWRC) field station in Gainesville, Florida, researches into vulture-related problems (Avery 2004). Roosting Black and Turkey vultures create nuisance, health, and safety problems (such as electrical power outages), but the tendency of Black vultures to prey on livestock is the most serious problem. Conflicts with Black and Turkey vultures are reported in at least 15 States. Where Black vultures killed livestock, ameliorative action included the dispersal of a large communal winter roost in Virginia. The elimination of the winter roosts did not substantially alter vulture activity in nearby livestock rearing areas, as the vultures had several alternate roost sites. Also, there were cattle and sheep carcasses in the vicinity that enabled vultures to feed and maintain their presence. Collaborative research between the NWRC, the Virginia Wildlife Services and the Florida Farm Bureau continued on the factors for vulture predation on new livestock.

The impact of Black vultures on livestock is worth examining in more detail. Avery and Cummings (2004: 59) described Black vultures as 'a problem species for many livestock producers': with evidence going back decades (see also Baynard 1909; Roads 1936; Sprunt 1946; Lovell 1947). An old publication by Baynard (1909) in Florida is cited, which noted that 'Hundreds of young pigs, lambs, etc., are annually devoured by them.... I have had them come into my yard and catch young chickens' (Avery and Cummings 2004: 59). The main compiler of information on these incidents, the United States Department of Agriculture's Wildlife Services Program documents an increase in domestic animal attacks since 1997. From 1997 to 2002, 84% of reports were from Virginia, Florida, Texas, South Carolina, and Tennessee, with 13 other states accounting for the rest. More than half of these attacks involved young cattle.

For example, in Virginia, there were 115 incidents of black vulture contact with 1037 livestock animals (1990-1996) (Lowney 1999). The main action was a group attack by about 20 to 60 vultures, which pecked the eyes, rectum, genitals and nose of young lambs and calves, and sometimes of cows giving birth. Avery and Cummings (2004) observed Black and Turkey vultures in a farm in central Florida foraging in pastures where there was active calving and feeding on afterbirth and fresh calf droppings. There were attacks on newborn calves., with 20 to 40 vultures feeding on the bodies. It was uncertain if the calves were stillborn or the vultures had killed them. The heifer in both events was so badly injured that it had to be euthanized by the rancher. There was a third event, in which three Black vultures pecked at the hooves of a calf while it was being born. The mother was however, able to drive the vultures away (Avery and Cummings 2004).

The killing of small- and medium-sized vertebrates is comparatively rarer for Old World vultures (Houston 1994). For example, before 1990, the reports of Giffon vultures predating livestock in Spain were described as 'anecdotal' but from around 2006 possibly more reliable reports were made (Margalida et al. 2014: 3; see also Camina et al. 1995). These authors nevetheless acknowledge that the 'killing of livestock by griffon vultures is a relatively minor problem. Domestic species, mostly dogs, cause greater damage to livestock than vultures' (Margalida et al. 2014: 4).

Nevertheless, Margalida et al. (2014) document a similar problem to that of Black vultures attacking livestock in the United States, but in this case it concerns Griffon vultures in Spain. This is a problem that appears to have emerged in the mid 1990s. These authors acknowledge that there is little factual data on this problem, much of the information being media driven and politically, rather than scientifically relevant.

The changes in European agriculture over the 19^th and 20^th centuries, especially in livestock rearing contributed to the decline in the numbers of Griffon vultures (Donazar et al. 1996; Donazar et al. 2009a). Conservation policies were successful, as vulture populations have increased by about 200% over the last 20 years over Europe, especially in the Iberian Peninsula (Spain and Portugal, and also parts of southern France; see C. Arthur and V. Zenoni, unpubl. data, on the increase in vulture-related complaints in the French Pyrenees 1993 and 2009 in Margalida et al. 2014, see also Donazar et al. 2009b; Margalida et al. 2010). Vultures were increasingly seen breeding and feeding near human habitations and infrastructure. The consequences were wildlife-human conflicts, angering farmers but neglected by scientists (Margalida et al. 2011a).

Also important were changes in farming practice. The traditional farming system in Europe used grazed livestock, protected from predators by shepherds and dogs (Kaczensky 1999). In many mountainous areas, there are predation possibilities by smaller avian and mammalian predators (such as ravens and crows, hawks and eagles, vultures or foxes). Smaller predators targeted placentas after lambing, and weaker, sick or young animals, which would formerly have been protected by guard dogs or shepherds. For the Griffon vulture, the increase in population and the food and farm policy issues increased the likelihood of contacts with potential prey. The definition of 'attack' also varies. Vultures may eat the kills of other predators, or calves or lambs that died at birth, making it seem as though the vulture made the kill. The large size and flock feeding behavior of the Griffon, and the small size of the livestock consumed, allows the rapid consumption of the carcass, making it impossible for the farmers to determine the cause of the death (Margalida et al. 2014). Basically, the question is, did the vulture kill this animal?

Margalida et al. (2014) studied 1,793 complaints on Griffon attacks on livestock collected by the relevant Spanish authorities (1996 to 2010). The location of this study is important, because about 95% of the Griffon vultures in the European Union are recorded in Spain. The information on the attacks concerned mainly sheep (49%) and cows (31%) and horses (11%) and the birthing times (between April-June) of these animals. Most the complaints of vulture attacks occurred during this period (60%), after closing the supplementary feeding stations (36% of complaints). A majority of the complaints (about 69%) were actually rejected as the course of death was uncertain. Nevertheless, compensation payments totalled EUR 278,590 from 2004 to 2010.

The case study of north-east Spain, recorded most of the livestock attacks. This area also had 7,433 pairs of Griffon vultures in 2008 (27.3% of the Griffon vulture population in the European Union) (Margalida et al. 2010). There are also many domestic animals (about 709,294 cows, 3,236,333 sheep, 109,118 goats and 24,772 horses; see MAGRAMA 2012). At this location, most of the livestock is free ranging, in open land in mountains and plains during June-September due to the seasonal movement of people with their livestock between summer and winter pastures. There are also supplementary feeding stations for scavengers, using carcasses (Donazar et al. 2009b). In the past, dead animals were abandoned for vultures, but the incidence of bovine spongiform encephalopathy (BSE) in 2001, prompted the EU to promulgate Regulation [CE] No. 1774/2002) that restricted this practice. Later legislation passed in 2009 and 2010 allowed occasional disposal of carcasses for avian scavengers. The action created a shortage of domestic carcasses and a decline in the carcasses supplied to the Spanish feeding stations (about 80%), as sanitary methods also improved (Donazar et al. 2009a; Cortes-Avizanda et al. 2010; Margalida et al. 2012; Margalida et al. 2014).Vulture behavior may have been altered by the reduction in the food supply, increasing tolerance of human proximity (Donazar et al. 2009b; Zuberogoitia et al. 2010; Margalida et al. 2010, 2012; Margalida and Colomer 2012). Human complaints about vulture behavior peaked from 2006 to 2010, coinciding with the period of food shortage.

Margalida et al. (2014) reported a clustering of the reports against vultures, suggesting that factors for attacks or complaints may be locally derived. Local husbandry practices may be important, and individual problem vultures may have been behind the attacks (Linnell et al. 1999). Negative media attention resulted, with some people calling for the poisoning of vultures, while others favored more feeding centers (Hernandez and Margalida 2008, 2009; Margalida and Colomer 2012; Margalida et al. 2011a,b; Margalida 2012). The negative perception of the relationship between humans and vultures exemplified the development of conflicts between people and vultures, changing an ancient relationship (Margalida et al. 2014: 4). Suggestions for the amelioration of the conflict included the use of livestock protection dogs (Espuno et al. 2004; Shivik 2006).

A close relationship between vultures and livestock farming has also been recorded in Asia. In a study of Nepal, a nation with six resident vulture species (White-rumped, Slender-billed, Egyptian, Red-headed, Himalayan Griffon and Bearded vultures; the Cinereous vulture is a winter visitor and the Eurasian Griffon vulture a passing migrant), vulture populations have declined, due to several factors, one of which is the decline in large domesticated and semi-domesticated livestock (Shrestha and Prasad 2011). The Water Buffalo (Bubalus bubalis Linnaeus 1758) is a huge bovid common in southeast Asia, which may be wild, semi-domesticated or domesticated. Historically, vultures were scavengers of buffalo carcasses, which were large enough to satisfy their needs. Other animals on which vultures fed were domestic cattle and goats. In recent times livestock numbers have declined, as farmers have moved to other businesses. Only goat rearing has remained popular, due to the more rapid renumeration. Vulture numbers have declined, resulting in the establishment of a 'vulture restaurant' by the Kalika and Jhulke Community Forest User Groups (CFUGs) (Shrestha and Devkota 2011).

In Turkey, which has the second largest population of the Cinereous vulture (after Spain), livestock are the largest dietary source for this species. Of these, sheep were dominant (76.6% of all pellets examined), followed by wild boar (44.1%) and chicken (22.5%) (Yamag and Gunyel 2010). 'This shows that livestock plays an outstanding role in the diet of the Eurasian Black vulture, and underlines its dependence on extensive livestock farming and grazing' (ibid. 15). The relationship between vultures and livestock is complicated by the fact that it is illegal to dispose of livestock carcasses in natural areas, so dumping is done illegally in fields (Yamag and Gunyel 2010). In addition, there has been a recent decline in cattle farming (TUIK 2010). There are virtually no alternatives to domestic livestock.

Moreno-Opo et al. (2010) also found extensive dependence on livestock among Cinereous vultures in Spain, and went further by examining what factors attracted this species to carcasses (see also Costillo et al. 2007b). The results showed that the number of vultures attending a carcass was related to the biomass and type of meat. The Cinereous vultures were attracted to carcasses with 'individual, medium-sized muscular pieces and small peripheral scraps of meat and tendon' (Moreno-Opo et al. 2010: 25); large morsels from large animals, and 'the carcasses of wild ungulates (natural and non-natural mortality through hunting practices)' (see also Donazar et al. 2009a,b). In the past, there was the traditional muladar, where carcasses of livestock were placed for the scavengers to remove. The food of the Cinereous vulture was in the past rabbits, sheep and wild ungulates, and also livestock (see Hiraldo 1976; Corbacho et al. 2007). Due to the environmental changes over the past three decades, the rabbit component of their diet has declined, and the livestock component has increased (see also Corbacho et al. 2007; Costillo et al. 2007b). The Cinereous vultures in the study were attracted by scattered, small- or medium-sized remains and large carcasses. At the former, the Cinereous vultures fed faster than at the latter. This favored communal feeders such as the Griffon vulture (Moreno-Opo et al. 2010). Therefore, both vulture species feed on livestock sized carcasses, but possibly the Griffon favors larger bovid carcasses.

In Africa, as was discussed in Chapters 1 and 2, and Part 2, vultures are primarily denizens of the savanna and are largely absent from the forests; the only common exception is the small Hooded vulture which may occur in forested towns such as Kumasi in Ghana (Campbell 2009). As described by Houston (1985: 856) 'The Old World vultures are confined to open habitats such as savannas, grasslands, and semideserts, and none of these species is found in any of the forested areas of Africa or Asia.' In the savannas of Africa, domestic cattle are a principal food source, especially in West Africa where there are fewer larger wild ungulates than in East Africa. This cattle herding culture in the savannas of West Africa enables the larger vultures to be present in large numbers (Scholte 1998; Wacher et al. 2013).

Cattle herding has been practiced in Africa for thousands of years. Most cattle are descended from Bos taurus indicus (Linnaeus, 1758), the humped Zebu from South Asia (Deshler 1963). Fossil, archaeological, historical and social sources have been used to uncover the origins of West African cattle (Doutressoulle 1947; Epstein 1971; Smith 1980; Muzzolini 1983; Epstein and Mason 1984; Shaw and Hoste 1987; Clutton-Brock 1989; Blench 1993). Traditional cattle herding, or pastoralism, was a subsistence lifestyle based on tending livestock herds, which produced meat, milk, blood, manure and traction. Traditionally, the nomadic pastoralists, mostly of the Fulani tribes, moved north into the Sahel and northern Sudan savanna during the rainy season, and southwards to the southern Sudan savanna during the dry season (Campbell 1998). An important consideration for cattle rearing in West Africa is the disease trypanosomiasis that kills animals and people, caused by protozoa of the species Trypanosoma brucei and carried by the tsetse fly (Murray et al. 1982). The protozoa lives in the blood of the animals and spreads with the bite of the fly. Tsetse flies include all the species of the genus Glossina, in the family, Glossinidae. Species that transmit the disease include Glossina morsitans, G. swynnertoni, G. pallidipes, G. palpalis, G. actinides and G. fuscipes. This disease is largely found in moist areas, such as the forests of central Africa, which is a major factor for the absence of cattle herding in the forests.

Some cattle breeds are more tolerant of trypanosomiasis than others. Trypanotolerant cattle breeds are the Hamitic Longhorns (N'Dama) and the Shorthorns. The N'Dama, indigenous to the Fouta-Djallon highlands of Guinea, is the main breed in western West Africa. Domesticated about 8,000 years ago, it acquired resistance towards trypanosomiasis (i.e., trypanotolerant) and other local diseases (Foy 1911; Chandler 1952; Desowitz 1959; Murray et al. 1982). Another breed, the Zebu, is found largely to the east of the N'Dama along the Sudano-Sahel belt. It has been crossbred with some other local breeds. Unlike the N'Dama, it is often affected and sometimes killed by tranpanosomiasis (Campbell 1998; Dwinger et al. 1992). Shorthorn cattle, also trypanotolerant are also present to the south of the range of the Zebu in the Guinea savanna belt. There are two variants. The larger savanna type is found in the Guinean or Sudano-Guinean savannas from Cote d'Ivoire to Cameroon; and the smaller Dwarf (Forest) Shorthorn is found in forested and coastal areas. Goats and sheep are also found in cattle rearing and farming areas. The historic breeds are the West African Dwarf goats (Capra aegagus hircus Linnaeus, 1758) and sheep (Ovis aries Linnaeus, 1758), which are mostly trypanotolerant (Adeoye 1984). Being fast breeders, these were important protein and supplementry income sources for the shifting cultivators and nomadic herders (Campbell 1998).

In the west-central African savanna of Chad and Niger, Wacher et al. (2013) found associations between Ruppell's Griffon vultures (the commonest), Lappet-faced vultures, White-headed vultures, White-backed vultures, Hooded vultures and Egyptian vultures and the density of livestock. In most parts of the study area, livestock outnumbered the wild ungulates; in a few areas wildlife reached similar density, mostly Dorcas Gazelle and a few Dama Gazelle, Barbary Sheep and Addax. The landcover in this area was of flat plains, including Sahelian grasslands and the light woodlands of the northern Sudan savanna.

In terms of individual vulture species presence, the Egyptian vultures in this study were present near rocky, desert outcrops and grasslands, in association with cattle herders, cattle near Hyphaene palms and livestock carcasses. The Hooded vultures were found in the southernmost areas, in association with more watered Sudan savanna, and close to human settlements and abattoirs. White-backed vultures were also found in the southern wetter, Sudan savanna, usually in association with livestock, and with other vultures mostly Ruppell's vultures and to a lesser extent Hooded and Lappet-faced vultures. They also moved north into the dryer Sahel during the rainy season. The Ruppell's Griffon vulture was found and associated with livestock throughout the Sahel and Sudan savannas under consideration, nesting in rocky inselbergs and trees.

This study points out that the close association between vultures and humans in the Sahel is due to 'high reliance on livestock carcasses.' Vultures were recorded at carcasses 21 times; the carcasses were those of cows (4), sheep or goats (6), camels (7), donkeys (3) and dorcas gazelle (1). The authors corrected the carcasses for body size differences by using the normal live weights of adults of each mammal species and concluded that 'livestock potentially contributed more than 99% by mass to vulture food sources' (Wacher et al. 2013: 197).

Hooded vultures in southern Ghana occur in close association with urban abattoirs and other meat processing areas, with little association with cattle herding in the coastal savanna. The cattle herds in the coastal savanna are small, with few carcasses for vulture consumption (Campbell 2009). Therefore, they congregate to eat the discards from abattoirs and meat markets in urban areas. The large wildlife of the coastal savanna of Ghana are largely extinct. The Hooded vulture is the only vulture species in this savanna, as the larger vultures such as the White-backed vulture and Ruppell's Griffon are confined to the northern savannas were ungulates are more common and cattle herds are more numerous.

Vultures, by eating cattle and other livestock carcasses, may also benefit people. The beneficial impact of vulture presence is most clearly seen when vultures are locally extinct, usually leading to increased but usually less effective scavenging by facultative scavengers, increased incidence of disease from the larger numbers of rotting carcasses, and possibly changes in human cultures that had adapted to vulture roles. For example, in the local extinction of vultures in parts of Asia, which will be examined in the next chapter in more detail, Pain et al. (2003) noted several unpleasant effects of vulture absence from areas where they were previously very common. Firstly, there was a great increase of small, predatory mammals, e.g., feral dogs and rats (Rattus spp.), which have high reproductive abilities. An example is cited of a carcass dump in western Rajasthan, India, where the dogs increased from about 60 in 1992 to 1200 in 2000. These created problems for nearby human settlements, increasing dog attacks on people, infectious diseases, livestock, and wildlife. Diseases, such as rabies and bubonic plague, are endemic and common in India and dogs and rats are the primary reservoirs. India has one of the highest rates of human deaths due to rabies in the world (World Health Organization 1998). Diseases that may spread from dogs and rats to wildlife and domestic livestock include canine distemper virus, canine parvovirus, and Leptospira spp. bacteria. As most facultative scavengers are predators, there may be higher predation pressure on wildlife when these scavengers replace vultures.