Old World Vultures and Mammal Scavengers

This section looks at the relationship between Old World vultures and mammal scavengers, in particular hyenas, jackals, lions, tigers, leopards, wolves, feral dogs and bears. As noted by Kendall et al. (2014: e83470) for scavengers, unlike predators 'food availability is a factor of not just prey density but also prey mortality rate, which will vary both spatially and temporally.' Therefore, the vultures have a relation not only with mammal scavengers, but also with the predators that will kill the prey to provide the carcasses. Mammal scavengers such as hyaenas and jackals in Africa and Asia are also capable of killing herbivores, so their relation is also as predators.

The relations between vultures and mammal scavengers are essentially those of competitors, while the relations between vultures and mammal predators are based on the latter's status as both providers and occasional competitors. All these animals may also be competitors either over unfinished kills or when they take over carcasses upon which vultures are already feeding. The other relations are with scavenging hyaenas, jackals, hunting dogs and other carnivore/facultative scavengers, which compete with vultures over the remains of the predators kills and may fight for their own kills when vultures surround their unfinished meals. Mammal scavengers usually dominate vultures, although in some cases scores or hundreds of vultures, may intimidate smaller mammals such as jackals into leaving the carcasses. In some cases, the larger vultures may attack jackals at carcasses, as numerous photographs published online attest (see for example Perry 2007).

Vulture relations with mammal scavengers are most important in Africa (especially East Africa) because it still has high densities of large wildlife and few human-created carrion sources (Wilcove and Wikelski 2008; Dobson et al. 2010; Kendall 2012). Large mammal carnivores are now commonest in Africa, especially the game parks of eastern and southern Africa. In Asia, and especially Europe, large carnivores are rare, with wolves, bears and tigers extinct in most areas. In Europe and Asia, despite the persistence of a few large ungulates such as the elk, livestock have slowly become the main source of food for many vultures. There are also vulture restaurants where livestock carcasses are dumped for vulture consumption (Green et al. 2006; Gilbert et al. 2007; Donazar et al. 2009, 2010; Cortes-Avizanda et al. 2010; Margalida et al. 2011).

Vultures are commonly seen as having an advantage over mammal scavengers, because their flight allows earlier arrival at carcasses (Houston 1974b; Mundy et al. 1992). While this is true, Houston (1983) also records a study where 64 carcasses were placed in the Serengeti to record the sequence of arrival of scavengers. The result was that no mammals arrived at 86% of the carcasses, despite vultures taking an average of two hours to reach the kills. 'This implies that vultures do not gain an advantage over mammalian scavengers just because they get to carcasses first. Their advantage is that they find caracsses that the mammalian scavengers often never reach at all' (Houston 1983: 143).

Vultures also use their flying skills to follow potential food sources more easily than mammals can, as some mammals, e.g., lions and hyenas are territorial, and consequently cannot follow ungulate movements over long distances (Schaller 1972; Kruuk 1992). Griffons, by contrast do not have feeding ranges and forage very widely, and have adapted to the vast herds of past African environments (Houston 1974b, 1983). Kendall's (2012) study identifies vultures as following migratory herds of large ungulates in East Africa (see also Pennycuick 1972; Houston 1974a, 1974b; Pennycuick 1983). This indicated that social vultures (Gyps spp.) were dominant and their numbers were higher during the presence of migratory ungulates in the dry season. These ungulates may be killed by lions and to a lesser extent leopards and cheetahs. Lions are the largest predators, they harvest the most meat and leave the largest carcasses, such as buffalo, wildebeest, zebra and even young rhinoceros and hippotamus, which they must defend against scavengers like hyenas, rather than against the subordinate carnivores (Cooper 1991). Leopards and cheetahs usually hunt smaller prey, such as antelopes and gazelles, and occasionally the warthog. Leopards commonly hide their prey in tree branches to avoid larger predators or packs of hyenas or African hunting dogs. Cheetahs, which cannot climb trees due to the lack of retractile claws, must feed out in the open and are thus vulnerable to competition from the large carnivores and facultative scavengers.

Some studies have shown that vultures prefer carcasses that died of causes other than being killed by carnivores. Kendall et al. (2012) document scavenger competition in the Mara-Serengeti ecosystem in Kenya. An important finding was that 'regardless of the predator's identity, presence of a predator reduced the number of vultures, suggesting that vultures prefer carrion not killed by predators where available' (ibid. 523). This result was also found by Houston (1974b) who estimated that 88% of the food consumed by vultures was of animals not killed by predators, possibly as a prior predatory feast would reduce the meat available and increase the likelihood of conflict with mammalian predators and scavengers.

Predatory mammals in East Africa frequently engage in scavenging (Hunter et al. (2006). Examples include lions, spotted hyaenas (Crocuta crocuta), black-backed and golden jackals (Canis mesomelas and Canis aureus), and less commonly in leopards (Panthera pardus) or cheetahs (Acinonyx jubatus) (Kruuk 1972; Schaller 1972; Houston 1979; Caro 1994). Large carcasses may attract more scavengers, as they last longer than smaller carcasses (Blumenschine 1986). Large carcasses in open areas are also more likely to attract scavengers and hence scavenger competition, because they are more visible than those in forest (Blumenschine 1986; Dominguez-Rodrigo 2000). Although mammals have a sense of smell, Old World vultures, unlike the Cathartids have no sense of smell and rely entirely on vision.

Cheetah kills are different from lion kills, as the lions are much larger, they tend to hunt and eat in groups, and may defend the prey for long periods using their superiority over all scavengers (Hunter 2006). Cheetahs are smaller, usually solitary or in pairs, are not dominant over the large mammal scavengers such as the spotted hyena, they usually do not defend the carcass and they tend to leave their kills early (Houston 1979; Hunter et al. 2006). Leopards may hide their kills in trees. Kendall et al. (2012: 528) found that 'vulture abundance was particularly low at leopard kills.'

The study by Hunter et al. (2006) of 458 kills that were observed in entirety (from the cheetah killing to the end of the scavenging), showed that vultures appeared at 32% (147 kills), spotted hyaenas at 15.5% (71 kills) and lions at 3.3% (15 kills). For a subset of 282 kills, jackals were also present at 14.2%. For 431 kills scavenger arrival was observed and at 69 (12.9%) of these cheetahs were driven away from the kill by the scavengers. These dominant acts were by spotted hyenas (54 of the 69, i.e., 78%), lions (15%), other cheetahs (3%) and by non-scavengers, such as tourist interference, warthogs (Phacochoerus africanus), baboons (Papio anubis) (4%).

Scavengers were generally unaffected by the time of the day of the cheetah kills. They were more attracted to larger carcasses and were as likely to appear at carcasses on the open plains as in the forest savanna—boundary. One important finding was that medium-sized vultures were more likely to scavenge on kills on the plains than the forest savanna—boundary and hyenas and lions were more attracted to kills in shorter grass. All size classes of vulture—large (Lappet-faced and White-headed), middle (Ruppell's griffon and White-backed), small (Hooded and Egyptian vultures)—were positively correlated in arrival at carcasses, with middle-sized vultures slightly more likely to be first. All vultures could arrive before or after hyenas.

Hunter et al. (2006) found some contrasting results from other studies. For example, although larger vultures have been documented as late arrivals at carcasses, due to their need for strong thermals (Pennycuick 1972; Houston 1975), in the current study there was no evidence of this. Also, despite the fact that Kruuk (1967) described the medium-sized Gyps vultures as arriving after the Lappet-faced and White-headed vultures, Hunter et al. (2006) found the opposite result, with medium-sized vultures more likely to arrive before their larger competitors. However, the study agreed with Houston (1974) that the griffon vultures located carrion by sight, as the Gyps vultures were less likely to arrive at kills in the forest savanna boundary. There was also minimal support for the evidence that the smaller vultures arrived late at kills (Kruuk 1967).

The Spotted hyena is decribed in most studies as predominantly a scavenger (Pienaar 1969; Waser 1980). However, they actually hunt for most of their food (Kruuk 1972; Tilson and Henschel 1986; Cooper 1990; Gasaway et al. 1991), despite a strong propensity for daytime scavenging (Kruuk 1972). Some studies have stated that hyenas may locate carrion by watching vultures descending to carcasses (Mills and Hofer 1998). Hunter et al. (2006) found that the spotted hyenas were likely to arrive earlier than vultures for kills which they took from cheetahs early (<5 minutes after the kill) possibly because they witnessed the kill. Where scavengers acquired cheetah kills after a longer period, hyenas were more likely to arrive after vultures, possibly because they were more likely to be attracted by the sight of descending vultures. This tallied with the work of Kruuk (1972: 146), where links between vultures and hyenas were described as 'a complicated relationship of mutual benefit and competition.' Hyenas may provide vultures with opportunities by driving the predator from carcasses and may also use vultures as visual cues for carrion (Hunter et al. 2006).

Black-backed and Golden Jackals are also common scavengers in the eastern African plains. Some studies indicate that jackals principally forage for small vertebrates and some plant materials, and are not primarily scavengers (Lamprecht 1978; Blumenschine 1986), while other studies indicate that jackals are in intense competition with vultures (Kruuk 1967). Houston (1979) used faecal evidence and found that only 3% of jackal diets comprised carrion (Houston 1979). Hunter et al. (2006) found them in some association with vultures, but unlike the lions and hyenas they did not follow the vultures to kills.

Lions are recorded as primarily predators, but also opportunistic scavengers (Schaller 1972; Houston 1974). In the study by Hunter et al. (2006) lions were invariably able to drive the cheetahs off the carcasses. Although this study did not record lions and hyenas together, other studies have shown that lions and hyenas compete for carcasses (Kruuk 1972; Schaller 1972; Cooper 1991). The relationship between the vultures and lions was similar to that of the vultures and hyenas, vultures tended to arrive before the mammals when the carcass was acquired late and after the carnivores when the carcass was acquired early.

In Europe, the main predators that scavenge on carrion are wolves, foxes and bears. Cinereous vultures have been described as dominant over foxes at carcasses (Brown and Amadon 1986). Few studies have examined the relation between wolves or bears and European vultures such as the Cinereous, Griffon and Egyptian vultures. The European Wolf subsists on livestock and garbage where human populations are high. It also eats moose (Alces alces Linnaeus 1758), red deer (Cervus elaphus Linnaeus 1758), roe deer (Capreolus capreolus Linnaeus 1758), wild boar (Sus scrofa Linnaeus 1758), mouflon (Ovis orientalis Linnaeus 1758), saiga (Saiga tatarica Linnaeus 1766), wisent or European bison (Bison bonasus Linnaeus 1758), ibex (Genus Capra Linnaeus 1758), chamois (Rupicapra rupicapra Linnaeus 1758), musk deer (Genus Moschus Linnaeus 1758) and fallow deer. They also prey on reindeer (Rangifer tarandus Linnaeus 1758) and fallow deer (Dama dama Linnaeus, 1758), but these species occur largely north of the range of any vulture species (del Hoyo et al. 1994; Peterson and Ciucci 2003).

Concerning the impact of vultures on facultative scavengers, Ogada et al. (2012) in a Kenyan case study investigated whether declining vulture numbers at carcasses would result in the longer existence of carcasses and if this would increase the numbers and contacts between the facultative scavengers. The evidence hinted that with a decline or absence of vultures, the mean carcass consumption rates almost tripled, there was a tripling of the average number of mammals at the carcasses and the mean time spent by these mammals at the carcasses also increased almost three-fold. There was also a near tripling of the average number of contacts between mammals at the carcasses. Other researchers report that vulture decline or extinction contributed to increased numbers of other scavengers (Selva and Fortuna 2007); these in the African savanna, would be hyenas (Crocuta crocuta, Hyaena hyaena) and jackals (Canis mesomelas) (Kruuk 1972; Kingdon 1997).

In India, researchers have found that vulture absence has possibly led to an increase in the population of rats and feral dogs (Rattus rattus) (Pain et al. 2003; Prakash et al. 2003; Selva and Fortuna 2007). These facultative mammalian scavengers perform a similar role as vultures in finding and consuming carcasses before decomposition (Sekercioglu et al. 2004). The change from vultures to mammals may affect disease transmission, as the decomposing carcasses serve as incubators for many pathogens, which infect contact mammals (Wobeser 2002; Butler et al. 2004; Jennelle et al. 2009). These carcasses may then serve as centers for the spread of diseases, as increased numbers of mammals may share carcasses, and contacts may involve aggression (Mills 1993; Ragg et al. 2000; Ogada et al. 2012). In Africa, hyenas and jackals may increase and these species play host to many pathogens that may infect many other wild and domesticated species (Alexander et al. 1994; Harrison et al. 2004). Diseases include rabies and canine distemper, the two common carnivore diseases of Africa. These may spread through contact between infected and un-infected animals often at carcasses (Mills 1993; Roelke-Parker et al. 1996; Butler et al. 2004).