Vultures, Cultural Landscapes and Environmental Change

Vultures and Urbanization. As noted by Campbell (2009: 341), 'a central, emerging research problem concerns the mutual co-evolution of the human-avian relationship, and how this is manifested in different land uses within the urban areas. Urban development impacts on vultures in several ways; positively in terms of food provision (road kills, human discards), buildings and green spaces for nesting, and negatively through habitat loss, noise, pollution, shooting, lower biodiversity and absence of food. Vultures in urban areas must adapt to intensive human presence and also to total landscape change, and in some cases new competition from corvids and Larus gulls. As was described in the first three chapters, different vultures react to urbanization in different ways. In this chapter we consider the species that are attracted to urban areas, followed by those that are minimally affected, and finally those that are not known to frequent urban areas, and may be locally extinct due to urbanization.

Among the New World vultures, the Black vulture has adapted well to urbanization. Black vultures are increasingly common in urban environments, increasing conflicts with people (Novaes and Cintra 2013; see also Buckley 1999; Avery 2004). Problems include property damage, roosting pollution due to defecation and aircraft collisions (Lowney 1999; Avery and Cummings 2004; Blackwell and Wright 2006).

Rubbish or garbage dumps are important factors for Black vulture presence. In some cases, a consequence of urban foraging by Black vultures is the ingestion of artificial products. For example, a study by Elias (1987) using defecated pellets found synthetic products, mostly plastic from bags in 39.1% of the total pellets examined. A study by Novaes and Cintra (2013) on Black vultures in Manaus (metropolitan population 1.8 million inhabitants), in the Central Amazon of Brazil, found that Black vultures scavenged in street markets, garbage dumps, open sewers and polluted streams. They also visited thermal power plants and roosted in vegetation remnants close to the feeding areas. 'Black Vultures adjusted to the nearest possible roost to the food source to reduce the cost of movement' (ibid. 1). Most roosting was in vegetation remnants, ranging from very small (0.31 ha) to very large (773 ha), and possibly because of the large number of such sites, nests in other areas were rare. Black vultures were able to roost in very small vegetation patches, where there was intensive human activity (such as street markets) when the roosts were near large garbage containers. By contrast, proximity to areas of thermal power for soaring was relatively irrelevant for roost site selection probably because the Black vultures approached the feeding site flapping rather than gliding on thermals (see also Buckley 1997).

Another study by Hill and Neto (1991: 173) found that, as skyscraper nesting is common in Brazil, 'The Black Vulture has benefited immensely from human post-Columbian colonization of the New World... feeding on the garbage of dumps, fish killed in polluted waters, livestock dying in pastures and animals killed along highways, the Black Vulture's numbers have increased so dramatically that it is now considered the most abundant bird of prey in the Western Hemisphere.' Cited examples of Black vultures in urban areas of Brazil include two nestling Black vultures on the 22nd floor window-ledge planter of a 23-story office building in downtown Sao Paulo, Brazil. The planter was 15 m long, 1.3 m wide and 12 cm deep. Other examples were of a nest with two eggs which later fledged on the 19th floor window-ledge planter (80 cm by 60 cm) of a condominium; and two other nests, one with two eggs in a roof recess of a tall Curitiba building.

Hill and Neto (1991; 175) point out that 'Skyscraper-nesting by the Black vulture appears to be common in Brazil. According to Dr. Werner Bokermann, Curator of Birds at the Sao Paulo Zoo and Dr. Lfizaro Puglia, Director of the Sorocaba Zoo (pers. comm.), 'nestling Black vultures are commonly brought into their facilities by the general public who report finding them on the window ledges of city buildings or underneath large roof-mounted water storage tanks.' They further note the possibility that the Black vulture population will increase further, with the increasing human population. The natural nesting sites are increasingly scarce. Hence, 'the increasing use of skyscrapers as nesting sites by Black vultures should be expected, due to the similarities that large, unkempt window planters and roof recesses have to natural cliff ledges and caves' (ibid. 176).

Some recommend the reduction of Black vulture in urban areas (Novaes and Cintra 2013). Methods include the reduction of their food supply, usually by more complete garbage collection, changing the sewage collection systems, the replacement of open garbage cans with closed garbage cans and the cessation of indiscriminate garbage disposal by local communities.

Similar to the Black vulture, Turkey vultures forage and roost in urban areas. The main distinction is the Turkey vulture's less communal nature. Although Turkey vultures are recorded as roosting in large groups, they are usually solitary or forage in smaller groups than the Black vulture. Kiff (2000) writes that urbanization may reduce Turkey vulture populations, for example in California (see also Garrett and Dunn 1981; Unitt 1984), although there are records of Turkey vultures nesting in buildings (Valentine 1873). However, some Turkey vultures in southern and south-central Saskatchewan were observed nesting in abandoned houses in 1982, in the Aspen Parkland and Boreal Transition ecoregions of Saskatchewan, a phenomenon that increased in the mid-1990s as vulture numbers increased and habitated zones expanded. Nesting in such areas produced similar numbers of fledglings as elsewhere in more natural surroundings (Houston et al. 2007). Igl and Peterson (2010) also recorded Turkey Vultures nesting in an abandoned car.

Airola (2011) examined Turkey vulture presence in a large 67-ha park named William Land Park with large, old ornamental trees in urban Sacramento. Trees in the park included Deodora cedar (Cedrus deodara), Atlas cedar (Cedrus atlantica), Italian stone pine (Pinus pinea); London plane (Plantanus acerifolia); coast redwood (Sequoia sempervirens) and red- gum eucalyptus (Eucalyptus camaldulensis). Turkey vultures used roosts in the park throughout the year, with average numbers peaking for October at about 200, and lowest in April-May at 10 to 15 birds. In the mornings, the vultures circled above the park to about 100 to 200 m and then flew directly southwards, mostly uncultivated grassland habitat. It was observed that vultures generally showed no response to the 'low-intensity human activities beneath and adjacent to roosting trees, including use of a walking and running trail and golf course, the feeding of ducks in the pond' (Airola 2011: 5). In this case the impact on people was minimal, despite the large number of roosting birds. The few problems included feces and regurgitated pellets during the migration season.

None of the other New World vultures are common in urban areas. To repeat the information from the earlier chapters, the King vulture lives mostly in tropical lowland forests (below 1500 m-5000 ft) from southern Mexico to northern Argentina, and also savannas and grasslands, and swamps or marshes near forests and nests on the ground (Wood 1862; Brown 1976; Houston 1994; Schlee 1995; Ferguson-Lees and Christie 2001). The bird is a ground nester. Mountainous, gallery and flooded forest are the main foraging areas (Ellis et al. 1983; Reid 1989). They also nest at the edge of undisturbed forest remnants. It remains when forest fragmentation occurs, if there are still large patched of forest (Stiles 1985). It does not adapt to human presence (Clinton-Eitniear 1986; Whitacre et al. 1991; Berlanga and Wood 1992).

The Yellow-headed vulture is also not known as an urban scavenger. It occurs in open terrain; freshwater or brackish and marshes, moist savannas, mangroves swamps, scrubland and scrub savanna, open and moderately forested riverine landcover and farmland (Ferguson-Lees and Christie 2001). In a case study in Brazil, it occurred only in savanna with lagoons (Zilio et al. 2013), while in Guyana it was reported in savanna grasslands, scrub or brush habitats, including white sand scrub, bush islands, and fresh water habitats, including lakes, impoundments, ponds, oxbows, marshes, and canals (Braun et al. 2007). Other habitats were forest edge and secondary pine-dominated savanna in Nicaragua (Martmez-Sanchez and Will 2010); uncultivated, mixed riverine and marsh vegetation in Brazil (Sick 1993); and near harvesting equipment in Mexico (Pyle and Howell 1993). Eggs are laid on in a tree hollow (Sick 1993) or on the ground in dense grass (Yanosky 1987).

The Greater Yellow-headed vulture is a forest species that avoids urban areas. It forages in the moist, dense, lowland forest, generally outside high- altitudes and non-forested areas (Hilty 1977; BirdLife International 2014). In Guyana, its habitat was lowland forest, including both seasonally flooded and non-seasonally flooded forest (Braun et al. 2007). Nest sites include cliff cave floors, in crevices or in tree hollows.

The condors are open terrain and upland specialists. The California condor is absent from urban areas rocky shrubland, coniferous forests, and oak savannas. When it was more numerous, an important former foraging habitat was the littoral zone of the Pacific Coast, which is gradually being recolonized by birds released from captivity (Nielsen 2006). Eggs are laid in cliff caves or crevices rocky outcrops or large trees are used as nest sites (United States Fish and Wildlife Service 1996). The Andean condor inhabits high, open terrain, such as grasslands, alpine meadows, rocky mountains up to 5,000 m (16,000 ft); and also lowlands in eastern Bolivia and southwestern Brazil, lowland desert areas in Chile and Peru and southern-beech forests in Patagonia (Sibley and Monroe 1990; Houston 1994; Parker et al. 1996; BirdLife International 2014). Eggs are laid on cliffs or rock ledges, or cavities scraped among boulders in relatively low areas or up to 5,000 m (16,000 ft) (Fjeldsa and Krabbe 1990; Haemig 2007).

Old World Vultures are also divided into urban invaders and those that avoid urban and human occupied spaces. African vultures are known to be present in cities, especially near abattoirs (Brown et al. 1982) Ssemmanda (2005: 10) notes that 'within urban centers they are generalist scavengers utilizing all kinds of waste associated with humans including human excrement, carcasses, offal, bones and fresh meat associated with slaughterhouses', thus removing organic waste. The Hooded Vulture is a known denizen of urban areas. Wacher et al. (2013) recorded this species near or over villages and towns, in line with its well-known commensal habits in West Africa (Brown et al. 1982). In this study, the Hooded Vulture was the only species recorded in towns, despite others of the six species observed being more numerous in the countryside (Ruppell's Vulture, Lappet-faced Vulture). Ogada and Buij (2011) describe the Hooded Vulture as extremely adaptable to any environment; e.g., deserts, forests, savanna and urban areas. It is a 'human commensal' that favors rubbish dumps and slaughterhouses in urban areas, one factor being the lack of competition from other vultures (Ogada and Buij 2011: 101; see also Anderson 1999). However, the disadvantage of this close relationship with people is the frequent killing of vultures for food and traditional medicines, especially in West Africa (Anderson 1999; Sodeinde and Soewu 1999).

In Guinea, most Hooded vultures observed were in towns, especially in larger cities like the capital Conakry and rural areas; none in protected areas (Richards 1982; Walsh 1987; Halleux 1994; Rondeau et al. 2008). The Hooded vulture is also fairly common in towns in Cote d'Ivoire (Demey and Fishpool 1991) and was previously common but now rare or absent from towns in Mali and Niger (Thiollay 2006a), and also Senegal, Sierra Leone, Togo (Ogada and Buij 2011). Older reports record it as common in Chad and the Central African Republic (Carroll 1988; Scholte 1998). It is strongly associated with towns in Ethiopia and South Sudan (Dellelegn and Abdu 2010; Ogada and Buij 2011) and still occurs in Malawi (Dowsett-Lemaire and Dowsett 2006). It is rare even in cities in other countries, such as Kenya, Tanzania, Zimbabwe, Lesotho, Mozambique and South Africa (Mundy 1997; Maphisa 2001; Parker 2004; Njilima et al. 2010; Ogada and Keesing 2010).

The Hooded vulture is also described as an urban vulture in Uganda (Ssemmanda and Plumptre 2011). In Uganda, the decline in vulture numbers is attributed to improved abattoir hygiene (Ssemmanda and Pomeroy 2010). Ssemmanda and Plumptre (2011: 17), note that 'across most of Uganda this is an urban dwelling species with the largest population in Kampala', this possibly partly due to 'new abattoirs in emerging towns that have attracted some of the birds.' It is also described as the only urban species among eight vulture species in Senegal and Gambia, the extreme western part of Africa (Barlow and Wacher 1997). Chemonges (1991) went further and wrote that 0.02% of the waste produced in Kampala, Uganda was consumed by Hooded vultures and marabou storks. Other scavengers were the Yellow-billed kite Gmelin, 1788, Pied crow (Corvus albus Statius Muller, 1776), Palm-nut vulture (Pomeroy 1975; Carswell 1986; Amuno 2001) and Egyptian vulture. The highest density of vultures were found near the Kampala Meat Packers (also termed the City Abattoir), where the largest slaughter house kills several hundred cattle and goats each morning. Items dumped at the back of the buildings are hooves, diseased parts, skin scrapings and surplus meat. The number of hooded vultures roosting in the vicinity increased from an estimated 124 in the early 1970s to 237 in 2001 (see also Pomeroy 1975; Amuno 2001).

In Burkina Faso, Hooded vultures and Black kites are more strongly associated with densely inhabited human settlements and refuse than with natural food sources and savannas (Thiollay 2006). Ogada and Buij (2011) describe past reports in which thousands of Hooded vultures were sighted near markets in Ouagadougou (the capital city of Burkina Faso) in the 1990s. These numbers have plummeted more recently. In Ghana, hundreds have been reported near the meat processing centres (Mundy 2000). Hooded vulture numbers increase with increased human presence during the academic session of the University of Ghana (Gbogbo and Awotwe-Pratt 2008). Vultures also nest in trees on the campus of the Kwame Nkrumah University of Science and Technology, in Kumasi, the second largest city in Ghana (Akyeampong et al. 2009).

A study by Campbell (2009) on the Hooded vulture in Ghana, found this species to be an urban specialist, that avoids rural areas. The hooded vulture is the only vulture species in the densely populated southern half of Ghana, with other, larger species confined to the northern half of the country (Mundy et al. 1992; Gbogbo and Awotwe-Pratt 2008). White-backed and White-headed vultures have been recorded in Mole in the northern savanna region of Ghana (Vermeulen 2011). Few studies have investigated the reason for the absence of the larger vultures (Ruppell's Griffon, White-backed vulture and White-headed vulture) from the more forested and populated southern half of the country, but possibly people and forests are a factor. In the south, the Hooded vulture's only scavenging rival is the Pied crow and to a lesser extent the Yellow-billed kite (Campbell 2009).

In this study Hooded vulture and Pied crow presence was positively correlated with human numbers, these species being most common in meat and waste production areas, and also places where there were street discards in non-food production and residential areas. Vultures were most common in meat markets, followed by vegetable markets, non-food markets, residential areas, rubbish dumps, central business districts, urban green spaces and finally, rural areas. Vultures and crows took meat pieces from butchers' tables, walked into windows and doors and flapped about people. In the meat production areas, vultures outnumbered crows, but were less mobile, circling or perching, rather than invading buildings as the crows commonly did. In the non-meat production areas, crows outnumbered vultures, and foraged in gutters, on sidewalks, public toilets, under vehicles, house windows and even piles of old clothing.

In the urban non-meat production areas, Hooded vultures and crows engaged in observational perching, hovering or low soaring, and dived to the ground to snatch human discards, refuse and dead rodents. Human discards included meal remnants, garbage and unwanted trade items. Vultures and especially crows also gathered in areas of human communal eating; crows appeared faster at snatching deliberately thrown food and outnumbered vultures three to one in such actions, creating sporadic nuisances, so people flapped cloths and papers at them, or even threw stones.

Regarding other species in Africa, information is minimal; possibly partly due to 'lack of active resident ornithologists' (Ssemmanda and Plumptre 2011). These authors note that much of the information is based on the Serengeti-Mara area (see also Kruuk 1967; Pennycuick 1972; Houston 1974, 1975, 1979). In the 1960s-1980s populations of vultures were larger, while in more recent times many species are now threatened. In Western and Eastern Africa, the Egyptian vulture is often migratory. There are also five resident species which, excepting the Hooded vulture are not recorded in cities. These are the Hooded vulture, African White-backed vulture, Ruppell's vulture, Lappet-faced vulture, and White-headed vulture.

Urbanization may be a factor for their extinction. For example, Margalida et al. (2007a) found that the Egyptian vulture was linked to availability of food and low human presence. Possibly other studies that showed that they were tolerant of humans were recorded in areas of higher vulture density (Ceballos and Donazar 1989). The Eurasian Griffon vulture was associated with the availability of food and landscape with low tree cover. The Bearded vulture was very selective, linked only to mountain environments with little vegetation cover for food, steep slopes for nesting and food preparation (ossuaries) and low human disturbance (an impossibility in and urban environment (Donazar et al. 1993; Margalida et al. 2007b).

In Asia, vultures are described as foraging in urban or other habitated areas, even if they roost away from habitation. Arun and Azeez (2004: 567) describe White-rumped vultures as using the waste dumps of urban areas as convenient 'fast food restaurants'. A study by Harris (2013) in Nepal describes the White-rumped vulture as foraging in human habitation and nesting in trees near habitation. The Indian vulture was 'found within cities, towns and villages associated with cultivated areas'. The Slender-billed vultures inhabited open forests up to 1,500 m in the vicinity of human habitation, scavenging at rubbish dumps and slaughter houses. The Redheaded vulture lived in open country near habitation and wooded hills.