The Role of Gulls as Reservoirs of Antibiotic Resistance in Aquatic Environments: A Scoping Review

Abstract

The role of wildlife with long-range dispersal such as gulls in the global dissemination of antimicrobial resistance (AMR) across natural and anthropogenic aquatic environments remains poorly understood. Antibiotic-resistant bacteria have been detected in resident and migratory gulls worldwide for more than a decade, suggesting gulls as either sentinels of AMR pollution from anthropogenic sources or independent reservoirs that could maintain and disperse AMR across aquatic environments. However, confirming either of these roles remains challenging and incomplete. In this review, we present current knowledge on the geographic regions where AMR has been detected in gulls, the molecular characterization of resistance genes, and the evidence supporting the capacity of gulls to disperse AMR across regions or countries. We identify several limitations of current research to assess the role of gulls in the spread of AMR including most studies not identifying the source of AMR, few studies comparing bacteria isolated in gulls with other wild or domestic species, and almost no study performing longitudinal sampling over a large period of time to assess the maintenance and dispersion of AMR by gulls within and across regions. We suggest future research required to confirm the role of gulls in the global dispersion of AMR including the standardization of sampling protocols, longitudinal sampling using advanced satellite tracking, and whole-genome sequencing typing. Finally, we discuss the public health implications of the spread of AMR by gulls and potential solutions to limit its spread in aquatic environments.

Wildlife and Antibiotic Resistance

“…Several wild animals do not travel long distances, hence contributing just to the local dissemination of AR. A different matter refers to migrating animals ( Figure 1 ), particularly birds that can travel long distances even between different continents ( Zeballos-Gross et al., 2021 ). Various studies have shown that the microbiomes of wild birds frequently contain human bacterial pathogens, including clones prevalent at hospitals, as well as ARB ( Oteo et al., 2018 ; Stępień-Pyśniak et al., 2019 ; Dec et al., 2020 ).…”

Dissemination and prevalence of plasmid-mediated high-level tigecycline resistance gene tet (X4)

“…In the latest report, researchers also detected the tet (X) variant genes in wild fish and shrimp ( Li et al, 2019 ; Concha et al, 2021 ). Wild animals were not directly exposed to clinical antibiotics, but more and more ARGs were detected in them, indicating wild animals including migratory birds, were likely to be involved in the large-scale exchange of ARGs, especially long-distance transmission of cross species ( Allen et al, 2010 ; Wang et al, 2017 ; Zeballos-Gross et al, 2021 ; Luo et al, 2022 ).…”

Climate Change Impacts on Microbiota in Beach Sand and Water: Looking Ahead

“…Bird population increase in beach settings is expected to lead to a potential increase in human exposure risk to pathogens such as Salmonella, Campylobacter and Chlamydia if populations continue growing in response to climate change [79]. These pathogens, in addition to other zoonotic disease-associated microbiota such as West Nile Virus, Aspergillus, Staphylococcus, and a variety of antimicrobial-resistant bacteria have been documented in gulls, terns, and barnacle geese [80][81][82]. These microbiota may be transmitted directly via deposition from the birds to coastal environments (sand and water), where they may accumulate and present human health risks.…”