Seasonal and spatial occurrence of zoonotic Salmonella serotypes in griffon vultures at farmland environments: Implications in pathogen pollution and ecosystem services and disservices.

Livestock production is a large source of microbial, pharmaceutical, and antimicrobial pollution worldwide. Vultures are one group of birds with particularly high exposure to food-borne pathogens due to frequent consumption of infected livestock carcasses. The potential origin and spatial-temporal shedding patterns of livestock-adapted Salmonella serotypes of zoonotic importance were evaluated in adult and nestling Griffon vultures (Gyps fulvus). We specifically assessed the exposure source and subsequent elimination of Salmonella-infected carcasses (ecosystem services) or transmission back to livestock (ecosystem disservices) by vultures, thus contributing respectively to disease mitigation or amplification in natural and farmed environments. The results show a seasonal high occurrence and turnover of a high variety of serotypes, especially swine-adapted ones isolated at high frequency. This suggests that vultures can be reservoirs and long-distance carriers of faecal Salmonella shed in supplementary feeding stations and breeding colonies. Contrary to their conservation purposes, feeding stations can act as Salmonella hotspots and reservoirs. However, a role for vultures in the transmission back to food-producing animals seems impossible because they do not come into contact at indoor farms, while transmission to free-ranging ruminants was not supported by the presence of ruminant-adapted serotypes in the vultures. Therefore, vultures do not promote disservices associated with the re-infection of livestock with Salmonella, but can provide quantitatively important ecosystem services by removing carrion contaminated with these and other zoonotic pathogens potentially affecting their health. Sanitary vigilance of the farms authorised to provide food for avian scavengers should avoid the disposal of swine and poultry carcasses with Salmonella and the antibiotics used to treat it. Extensive free-ranging livestock and their carcasses exploited in the countryside should be a priority for the conservation of vultures and their ecological function as cleaners and disease mitigators.