“Vultures As an Overlooked Model in Cognitive Ecology”, 2021-11-24 ():
[supplement; media] Despite important recent advances in cognitive ecology, our current understanding of avian cognition still largely rests on research conducted on a few model taxa. Vultures are an ecologically distinctive group of species by being the only obligate carrion consumers across terrestrial vertebrates. Their unique scavenging lifestyle suggests they have been subject to particular selective pressures to locate scarce, unpredictable, ephemeral, and nutritionally challenging food.
However, substantial variation exists among species in diet, foraging techniques and social structure of populations. Here, we provide an overview of the current knowledge on vulture cognition through a comprehensive literature review and a compilation of our own observations.
We find evidence for a variety of innovative foraging behaviors, scrounging tactics, collective problem-solving abilities and tool-use, skills that are considered indicative of enhanced cognition and that bear clear connections with the eco-social lifestyles of species. [Brain data from et al 2017]
However, we also find that the cognitive basis of these skills remain insufficiently studied, and identify new research areas that require further attention in the future. Despite these knowledge gaps and the challenges of working with such large animals, we conclude that vultures may provide fresh insight into our knowledge of the ecology and evolution of cognition.
[Keywords: foraging cognition, social cognition, socio-ecology, vultures]
…vultures exhibit signatures of complex cognition in the foraging and social domains. These include many cases of feeding innovations and cooperative behaviors (see details below). Third, vultures show a slow pace of life characterized by long periods of chick development, an extended juvenile period, delayed sexual maturity, low fertility and long live spans. Such a life history is expected to enhance cognition by facilitating the growth and development of enlarged brains and by increasing the net benefits of learning (reviewed in et al 2016). A long-life span also means that environmental conditions encountered early in life can largely differ from those found in the future, which may further select for enhanced flexibility in decision-making. Four, vultures show an unusual ecology. Vultures are the only obligate carrion consumers among terrestrial vertebrates (2001; Mundy et al 199232ya; van et al 2020a). Yet unlike previous model taxa used in cognitive research, which are all highly social, vultures have largely diverged in their social lifestyle.
Thus, this group offers a unique perspective to study the relative roles of social and ecological pressures in selecting for enhanced cognition. Finally, vultures comprise 2 distinct lineages, the New World vultures (Cathartidae, 7 species) and Old World vultures (Accipitridae, 16 species; Ferguson-2010) (Figure 2) that have independently converged to similar foraging habits. The existence of convergent solutions to similar problems is a major signature of selection, and hence finding similar patterns in New and Old World vultures may provide important insight into the selective processes that have shaped cognition.
…Most vultures are habitat generalists that live in a variety of natural environments, including rain forests, savannas, desserts and mountain areas. Within these habitats, different species often co-occur in the so-called vulture-guilds, in which species coexistence is facilitated by a number of morphological differences (body size, wing morphology and beak shape) and social adaptations (Figure 2). These socioecological differences are primarily associated with the differential consumption of carcasses varying in size and predictability (reviewed in van et al 2020a) which, in turn, confront them to contrasting cognitive demands. Vultures from the Gyps guild differs from all other vultures in their social lifestyle and foraging habits. They are highly social year-round, breed in cohesive or loose colonies and form large communal roosts. Foraging occurs in loose or highly dispersed groups, and they extensively rely on conspecifics to locate large carcasses of ungulates and livestock (Cortés- et al 2014; Dermody et al 201113ya; et al 2017; Jackson et al 200816ya), which are exploited through crowd-foraging (2001; Mundy et al 199232ya). All other vultures mainly search for carrion alone (or in couples) and display solitary to territorial breeding habits (reviewed in van et al 2020a).
…Studies on food remains in nests and anecdotal reports show that generalist foragers (both facultative social and non-social) consume almost any kind of carrion available. In addition to a wide diversity of birds and mammals, this includes reptiles, amphibians, fish and a variety of invertebrates such as mussels, shrimps, and insects (Ferguson-2010).
…Innovative foraging techniques: …Anecdotal observations suggest that the Black vulture possess exceptional skills for innovation. This species, but also the Turkey vulture, regularly engages in fishing activities, usually by catching dead or injured fish using their beak. In several occasions, individuals have even been observed performing actual dives, in which the body and head are completely submerged by water (Jackson et al 197846ya). There are also several reports of Black vultures cleaning other mammals to feed on ticks, organic debris, or even flesh from open wound ( et al 2018; et al 2018; 2007b, 2010). They also can feed on the placenta of sea lions by cutting the pup’s umbilical cord ( et al 2008). Although mutualistic in nature, these interactions seem to have a clear self-serving function. More intriguingly, Black vultures also frequently engage in interspecific allopreening with Crested Caracaras Polyborus plancus (Lopes 2008; 1984; Souto et al 200915ya). Black vultures have learned to open bags at garbage dumps and nowadays also dismantle bags left unattended by bathers at coastlines and in refuse containers (2007a). They are the only vulture known to have successfully colonized highly urbanized environments where it may scrounge for food within city streets, harass residents and also enter houses to steal food (2020). The great diversity and type of foraging techniques expressed by this species exceeds that of all other vultures and is quite unique even among birds in general.
…Scrounging tactics: …Indeed, analyses in birds have shown that kleptoparasitic tactics are more frequent in lineages that have larger brains relative to body size (Morand-Ferron et al 200717ya). Vulture scrounging tactics come about in many forms and can vary considerable in their complexity. Facultative social Turkey and Egyptian vultures display unique innovative scrounging tactics particularly suggestive of enhanced cognition. For example, an adult Turkey vulture was once observed beating up a heron nestling with its wings until it regurgitated food, which was then used to feed its own young (1967). Similar behaviors have observed in adult Egyptian vultures, which frequently steal regurgitated food at nest of Griffon vultures (1991) (Figure S1) and sometimes also harass nestlings to prompt food regurgitation (Fernández & Fernández-1994, authors unpublished)
…In highly non-social species, particularly in the Redheaded vulture Sarcogyps calvus and King vulture Sarcoramphus papa, there are claims suggesting that individuals can specifically keep track of the movements of solitary hunting carnivores (Panthera and Puma spec.) to feed on their fresh kills (2010; 2007). This would imply cognitive skills to interpret presence-absence cues of highly mobile individuals in dense vegetation, although compelling scientific prove for such abilities is lacking. In closed rain forest, king vultures have been also claimed to engage in transect soaring at high altitude to keep track of the activities of Cathartes vultures, which locate carrion by smell (1988). However, in other areas with more open vegetation king vultures are often the first to arrive at carcasses (1991). This points towards skills to detect food both independently and through inter-specific social information use.
…Collective problem-solving: …There is one observation suggesting that Griffon vultures can collectively reach individually unattainable food resources. While trapping Griffon vultures with a cage-trap [a metal construction, covered by a net, that vulture only can enter through a door (Figure S3)], they managed to consume several hundreds of kilograms of meat despite the cage-trap being closed. This was only possible if vultures gathered in large numbers on the top net of the cage, so that eventually, their collective weight allowed them reaching the food. However, the degree of coordination of the action performed does not necessarily need to be particularly sophisticated, and it remains unclear whether Griffon vultures had a clear understanding of the role of conspecifics to accomplish this foraging task.
There is another report of collective foraging, in this case hunting, in the facultative social Lappet-faced vulture Torgos tracheliotos. On various occasions, groups of 15–22 individuals were seen attacking together crèches of flamingos. Apparently, they did so by circling around the crèche, and taking their turn to catch hatchlings (2006). At a later stage, small groups of Lappet-faced vultures were observed to pursuit full-grown immatures in flight, to kill them and feed on this prey together. These seemingly well-coordinated attacks suggest capacities to interact cooperatively that resemble those of socially hunting carnivores.
Tool-use habits: … In vultures, the closely related Egyptian and Bearded vultures are both well known for their tool-use habits, involving true tool use, i.e. stone-throwing to open up eggs, in the former (Figure S4) (van Lawick-Goodall & van Lawick-1966), and proto tool-use, i.e. bone-dropping to fragment them for consumption, in the latter species (1976).
…There are some claims of Egyptian and Bearded vultures dropping turtles from the air (or even lizards) and/or for the use of stones to break open their shells in case of Egyptian vultures. However, we could not find detailed descriptions of turtle dropping in the literature.
…Claims also exist of Egyptian vultures using sticks to collect nesting material (Stoyanova et al 201014ya). Although this behavior has neither been verified, the observation of twigs with wool sticks is relatively common (Figure S6).
…Interestingly, escalated fights, although rare, often attract the attention of conspecifics (Supplementary Material video 3), suggesting that individuals actively keep track of social disputes and/or shifts in social rank.
…the observation that marked Griffon vultures with full crops often visit feeding stations on consecutive days, without participating in foraging activities (Acha et al 199826ya), suggests that individuals gather at food resources also for social purposes, possibly to collect public information about conspecifics.
…Like the social Gyps, the Black vulture has evolved crowd-foraging habits (2020). This facultative social species is renowned for its high-levels of aggressiveness. Despite being relatively small in size, the cooperation between individuals allows to displace from carcasses more powerful species such as Andean condors Vultur gryphus (Carrete et al 201014ya). Their foraging groups are thought to be composed of sub-coalitions of several breeding pairs and their offspring (Parker et al 199529ya). Group members maintain social ties through extensive allopreening (1987) and, presumably, they might also provide each other social support during feeding and at roosts (2020). Their crowd-foraging habits further stresses that this type of feeding strategy may not necessarily be indicative of poorly developed cognitive skills generally.
…Social bonds and cooperative partnerships: …Once mated, pairs of solitary breeding species (both facultative and non-social) form very tight partnerships. A number of striking examples in Egyptian vultures illustrate the well-developed cooperative skills among pair-members. In one occasion, a pair was seen cooperating to steal regurgitated food at a Griffon vulture nest; while one of the individuals distracted the fully grown nestling, the other snatched away part of the food (2017). In another occasion, a pair was seen feeding together on an abandoned egg of a Griffon vulture. In this case, the male searched for a suitable stone and cracked the egg, after which the female pecked it open with her beak ( et al 2015). In a last example, a female Canarian Egyptian vulture was once observed walking around restlessly with a piece of meat in her beak for more than 10 min at a feeding station. After noticing her partner, she handed over the food item to the male, which then flew away immediately, probably to feed their fully grown nestlings (Supplementary Material video 5, Figure S10). Cooperation has also been observed in other species. In the White-headed vulture Trigonoceps occipitalis, pair-members have been observed killing a live mongoose together, a technique that requires close cooperation (2014). In Redheaded vultures and the King vulture, pair-members are often observed arriving at carcasses simultaneously (2016; et al 2014).
…Cognition of vultures in other contexts: A last intriguing behavior of Bearded and Egyptian vultures, further adding to their unique behavioral repertoire, is their habit to deliberately stain feathers with red soil through mud bathing [cf. dust bathing] (Negro et al 199925ya; van et al 2017) (Figure S15, Figure S16). This highly unusual type of ‘cosmetics’ is not known in other birds (Delhey et al 200717ya). Although suggested to provide sanitary benefits (Arlettaz et al 200222ya) or to act as a signal of dominance (Negro et al 199925ya), none of these functions has so far been clearly proven ( et al 2019; van et al 2017).