INTRODUCTION

Cannibalism, or intraspecific predation, is widely observed in the animal kingdom (Fox, 1975; Ebensperger, 1998; Ontiveros and Pleguezuelos, 2014). In birds, cannibalism has been found in diurnal raptors (Ingram, 1959; Jones and Manez, 1990; Negro, et al., 1992, Boal and Bacorn, 1994), owls (Ingram, 1959), and colonial water birds (Smith and Munro 2008; Gubiani et al., 2012). Most of these cases have been observed during nest monitoring, and involve parental infanticide (Jones and Manez, 1990; Markham and Watts, 2007; Korňan and Macek, 2011; Solaro and Sarasola, 2012; Ontiveros and Pleguezuelos, 2014) or siblicide (Ingram, 1959; Bortolotti et al., 1991; Boal and Bacorn, 1994). However, cannibalism in the wild is rarely found, except in nests, because it is impossible to constantly monitor animal behavior without knowing when and in which species and individuals cannibalism might occur (Polis, 1981; Lecea et al., 2011, Ontiveros and Pleguezuelos, 2014). Aegypius monachus, the Cinereous vulture, is a typical winter migratory bird, which spends winter in Korea and summer in Mongolia (del Hoyo et al., 1994; Kim et al., 2007; NIBR, 2011; Kim et al., 2015; Kim et al., 2016). The species is classified as near threatened (NT) in the International Union for Conservation of Nature (IUCN) Red List, as there are only 2,300–2,500 Cinereous vulture pairs in Europe and 5,500–8,000 pairs in Asia (IUCN, 2017). Approximately 2,500 Cinereous vultures spend winter in Korean regions (e.g., Paju-si, Goseong-gun, Cheorwon-gun), forming groups of 100–500 (occasionally more than 1,000) individuals that rely almost exclusively on the artificial supply of livestock by-products (cow, pig, chicken, etc.) for survival (NIBR, 2011; IUCN, 2017). About 40–60 vultures spend winter in the Geumho wetlands, Haenam, South Korea, and their main sources of food include carcasses of water birds such as ducks or geese. They also feed on livestock by-products scattered around farmlands by directly locating them (NIBR, 2011). Here, this report provides the first case of cannibalism observed in Cinereous vultures with in a paddy field near Lake Geumho, South Korea.

MATERIALS AND METHODS

On 17 January 2017, for about one and a half hour (between 15:00 and 16:30), intraspecific predation was directly observed in Cinereous vulture Aegypius monachus in a nearby reed wetland close to a paddy field near Lake Geumho (34°35ʹ58.25ʺ N, 126°26ʹ57.64ʺ E) during bird-watching. To examine what the vultures were feeding upon, it was observed and recorded approximately 20 m (or 60 m) away from the site in the car, and after the last vulture finished feeding and flew away, the observer approached the feeding site and identified remains of the prey. The behaviour of vultures were observed using 10 × 30 binoculars (Swarovski CL) and photographed using a camera (Nikon D500) with a telephoto lens (Nikon AF-S Nikkor 400 ㎜ 1:2.8 DII), in order to record their behaviour.

RESULTS AND DISCUSSION

On 17 January 2017, around 15:00, five vultures began to soar in the sky and some soon flew down to the nearby reed wetland close to a paddy field near Lake Geumho (34°35ʹ58.25ʺ N, 126°26ʹ57.64ʺ E). When the observer approached within 20 m of the site by car, but, because the vultures had landed in a wetland about 1.5 m lower than the surrounding area, the reeds around the paddy field obscured the view. However, a high-pitched vulture cry could be heard from the reeds, and, using binoculars to look between the reeds from the car, seven vultures were found. Four vultures appeared to be fighting, and three of these were spreading their wings while holding down one vulture and pecking on it; this vulture was crying and spreading both wings, overturned on the ground. The other vultures standing nearby looked in the direction of the observer. Because fighting for food is a common behavior among vultures, this was not a major concern, although fighting when there was no food around (no traces of any animal carcasses, such as birds or mammals on the ground) was odd. In addition, the possibility of vultures killing a conspecific while it was alive was not anticipated, based on their dietary habit of eating dead animal carcasses and very rare reports of vultures preying on live animals such as lizards and insects (del Hoyo et al., 1994; NIBR, 2011).

When the observer was approximately 60 m away from the site, more vultures (about 20) gathered in the sky; minutes after, some flew down toward the site. The vulture cry reached a higher pitch and was more intense than usual; this higher pitch persisted for about 5 min (with the total duration of the cry being more than 20 min) more before it stopped. After for about 30 min, using binoculars, the observer looked at the vultures between the reeds to determine what happened to the vulture and realized that it remained overturned by other vultures but its wings were no longer moving and the crying had also ceased. Only then did evidence suggest that something unusual might have happened: at least nine vultures had been feeding on their conspecific. When the observer went back again within 20 m of the area where the vulture was being attacked, seven vultures began to emerge one after another from the reed wetland and sat and rested side-by-side on high ground; their filled crops indicated that they had fed sufficiently, and its remains were found. One was still pecking on the flesh from the skeleton (Fig 1). After the last vulture finished feeding and flew away, one vulture was still present, crouching at the site and unable to fly. The observer approached the feeding site and found remains of a vulture, including body feathers, skull, sterna keel, and both legs. The bones of wings and tail, as well as flight and tail feathers, and both feet were not pecked and eaten (Fig 2). The remaining skeleton was very fleshy, and the surrounding grass was wet with the blood of vulture. No other traces of a mammal or bird (feathers, fur, skeleton, etc.) that could have been the vultures’ prey were found.

Cannibalism (i.e., intraspecific predation) in nests, when food is scarce, significantly affects the breeding success of Eleonora’s falcons Falco eleonorae (Hadjikyriakou and Kirschel, 2016). A partial reduction of brood size by infanticide has occasionally been explained by constraints on food availability (Ingram, 1959; Jones and Manez, 1990; Solaro and Sarasola, 2012), although food shortage alone cannot explain infanticide (Solaro & Sarasola 2012). An extra nestling in a brood represents a reservoir of nutrients, and its consumption allows recovering part of the considerable energy used for reproduction in Bonelli’s eagles Aquila fasciata; however, cannibalistic parents might be considered as having an aberrant behavior in this species (Korňan and Macek, 2011; Ontiveros and Pleguezuelos, 2014). Other possible causes for infanticide might be the stress associated with breeding near humans or with the sensor camera set up for monitoring a nest (Fox, 1975; Solaro and Sarasola, 2012). However, a vulture directly attacking another live vulture and eating it is considered a very rare behavior for scavengers like Cinereous vultures.

The paddy field and wetland around Lake Geumho are overwintering grounds for migratory birds, and many ducks and geese spend winter here, feeding on the remaining grains and stems of rice after it has been harvested from October to March (Kim et al., 2015; Kim et al., 2016). Because vultures in the wetlands around Lake Geumho directly search for their prey in the wild, increasing or decreasing numbers of ducks and geese have a major impact on the overwintering vulture community (del Hoyo et al., 1994; Kim et al., 2015; Kim et al., 2016). The highest number of ducks and geese are found at the start of winter, between November and December, which is the period when it is most probable to find carcasses that become food for vultures (del Hoyo et al., 1994; Kim et al., 2015; Kim et al., 2016). However, as the number of ducks and geese decreases throughout mid-winter (January), the likelihood of finding food for scavengers like vultures decreases, causing them to go hungry for an extended period. Thus, cannibalism as observed in the present study might be due to such a decrease in available food resources (Lecea et al., 2011; Ontiveros and Pleguezuelos, 2014). In fact, a similar case was reported for the Eurasian griffon vulture, Gyps fulvus, in Spain (Lecea et al., 2011), when an individual was trapped, killed, and eaten by its conspecifics. In this case, however, it was not clear that the vulture was killed by its conspecifics, because the whole body of the vulture was not visible; this was because the other vultures were obscuring it from view. However, the observer saw one vulture crouching at the site that seemed almost incapable of flying and was very emaciated, suggesting that the vulture that became the prey might have also been exhausted when it was with this vulture. In addition, it seemed that the high-pitched cry that continued for about 20 min was not from a competitor, but the scream of the vulture. Somehow, the reduction of food resources might have increased intraspecific competition, and hence aggressiveness, leading to killing and consuming a conspecific (Lecea et al., 2011).

Overall, the cannibalistic behavior reported here, together with results from previous studies conducted on other raptor species, indicates that when food resources are scarce during wintering, vultures may become vulnerable to dehydration and to predation by conspecifics.