Urban yellow-legged gull (Larus michahellis) and peri-urban Audouin's gull (Larus audouinii) as a source of Campylobacter and Salmonella of public health relevance

Campylobacter spp. and Salmonella spp. are the leading cause of human enteric infections in the European Union. Some gull species act as reservoirs and play an important role in the epidemiology of these zoonotic agents. To gain insight into Campylobacter and Salmonella epidemiology we studied colonies of Audouin's gull (Larus audouinii) and yellow-legged gull (Larus michahellis) in Barcelona metropolitan area, Catalonia (north-eastern Spain). We assessed the occurrence, genetic diversity, virulence potential, and antimicrobial susceptibility of Campylobacter and Salmonella isolates recovered from gull faeces in different time periods within 2009-2018. The occurrence of Campylobacter was higher compared to Salmonella in both gull species. Also, the occurrence of both pathogens was significantly higher in Audouin's gull (45 % for Campylobacter, 20 % for Salmonella), than in yellow-legged gull (13 % and 7 %, respectively). All but one individual carried C. jejuni; the remaining positive yellow-legged gull carried C. lari. Salmonella serovar Typhimurium (including its monophasic variant) was the most frequent in both hosts followed by ser. Bredeney. Other serovars frequently associated with human salmonellosis (Infantis, London, Virchow) were only isolated from yellow-legged gulls. Multilocus Sequence Typing analyses showed that yellow-legged gull and not Audouin's gull carried several Campylobacter genotypes associated with human enteritis. Campylobacter isolates from both gull species revealed a high virulence potential, as opposed to Salmonella isolates which showed a lower prevalence of virulence-associated genes, particularly in Audouin's gull. Overall, a moderate to high frequency of antimicrobial resistance (including multidrug resistance) was found in both pathogens from both gull species. Campylobacter and Salmonella from yellow-legged gull showed a higher frequency of isolates resistant to antimicrobials of relevance in human medicine. Overall, our results highlight the potential public health threat associated with these gull species, particularly yellow-legged gull, in densely human populated areas.