Halogenated Flame Retardant Exposure Pathways in Urban-Adapted Gulls: Are Atmospheric Routes Underestimated?

Urban-adapted gulls can be exposed to flame retardants while foraging in landfills where elevated concentrations of polybrominated diphenyl ethers (PBDEs) and other halogenated flame retardants (HFRs) have frequently been measured in air. However, the contribution of atmospheric exposure has largely been overlooked compared to dietary exposure in birds and other wildlife. The overall objective of this study was to investigate the contribution of atmospheric exposure pathways relative to diet for PBDEs and other HFRs in ring-billed gulls (Larus delawarensis) nesting in the densely populated Montreal area (QC, Canada). Miniature passive air samplers (PASs) were deployed on the back of wild-caught ring-billed gulls for ten days. Concentrations of PBDEs and other HFRs were determined in PASs carried by ring-billed gulls as well as their lungs, stomach content, liver, preen oil, and onto the surface of their feathers. We evaluated the atmospheric and dietary exposure routes for the most abundant HFRs in samples using a structural equation model implemented in a Bayesian framework. Results indicated that lung concentrations of BDE-28 increased with its levels in air determined using bird-borne PASs. No association was found between BDE-28 concentrations in lungs and liver, whereas BDE-209 concentrations in liver increased with those in lungs. Moreover, BDE-28 and -47 concentrations in liver increased with those on feather surface, while liver BDE-47 concentrations were also positively related with those in stomach content. These findings suggested that, in addition to dietary exposure, atmospheric exposure pathways through inhalation and co-ingestion during feather maintenance (preening) significantly contribute to the accumulation of PBDEs in liver of ring-billed gulls. Atmospheric exposure to HFRs should therefore be considered in future landfill-foraging wildlife species as a potential exposure route compared to the traditional dietary exposure pathway.