Changes in thyroid function of nestling tree swallows (Tachycineta bicolor) in relation to polycyclic aromatic compounds and other environmental stressors in the Athabasca Oil Sands Region

• Published in: Environmental research 2019-02, Vol.169, p.464-475
• Main Authors: Fernie, K.J., Marteinson, S.C., Chen, D., Palace, V., Peters, L., Soos, C., Smits, J.E.G.
• Format: Article
• Language: English
• Subjects: Air pollution; Animals; Athabasca Oil Sands Region; Bird; Canada; Environmental Monitoring; Environmental Pollutants - toxicity; Multiple stressors; Oil and Gas Fields; PACs; Polycyclic Compounds - toxicity; Sand; Swallows - physiology; Thyroid function; Thyroid Gland - physiology; Tree swallows; Trees
• ISSN: 0013-9351; 1096-0953
• DOI: 10.1016/j.envres.2018.11.031

In the Canadian Athabasca Oil Sands Region (AOSR), nestling tree swallows (Tachycineta bicolor) raised near mining-related activities accumulated greater concentrations of polycyclic aromatic compounds (PACs) that contributed to their poorer condition, growth, and reproductive success. Here, we report changes in thyroid function of the same 14 day old (do) nestlings (N ≤ 68) at these mining-related sites (OS1, OS2) compared to reference nestlings (REF1), and in relation to multiple environmental stressors that influence avian thyroid function. Thyroid function was compromised for OS1 nestlings but generally comparable between OS2 and REF1 chicks. In 2012, circulating total triiodothyronine (TT3) and thyroxine (TT4) were similar among all nestlings. The OS1 chicks had more active thyroid glands based on histological endpoints. Hepatic T4 outer-ring deiodinase (T4-ORD) activity was suppressed in OS1 and OS2 chicks. Despite inter-annual differences, OS1 chicks continued experiencing compromised thyroid function with significantly higher circulating TT4 and more active thyroid glands in 2013. The OS2 chicks had less active thyroid glands, which conceivably contributed to their suppressed growth (previously reported) relative to the heavier OS1 nestlings with more active thyroid glands. Thyroid gland activity was more influenced by the chicks’ accumulation of (muscle), than exposure (feces) to naphthalene, C2-naphthalenes, and C1-fluorenes. Of four major volatile organic contaminants, sulfur dioxide (SO2) primarily influenced thyroid gland activity and structure, supporting previous findings with captive birds. When collectively considering environmental-thyroidal stressors, chicks had a greater thyroidal response when they experienced colder temperatures, accumulated more C2-naphthalenes, and consumed aquatic-emerging insects with higher PAC burdens than terrestrial insects (carbon (δ13C)). We hypothesize that the more active thyroid glands and higher circulating TT4 of the OS1 chicks supported their growth and survival despite having the highest PAC burdens, whereas the lack of thyroid response in the OS2 chicks combined with high PAC burdens, contributed to their smaller size, poorer condition and poorer survival. •Compromised thyroid function in tree swallow chicks evident in Canadian Oil Sands.•Increased thyroid activity, variably increased plasma T4 & suppressed liver enzymes.•Multiple environmental stressors compromise thyroid function of tree swallow ch