Feathers as integrated archives of environmental stress: Direct and indirect effects of metal exposure and dietary ecology on physiological stress in a terrestrial raptor

Abstract

Metal pollution is a global environmental issue with adverse biological effects on wildlife. Long-term studies that span declines in metal emissions due to regulation, resulting in varying levels of environmental contamination, are therefore well-suited to investigate effects of toxic metals, while also facilitating robust analysis by incorporating fluctuating environmental conditions and food availability. Here, we examined a resident population of tawny owls in Norway between 1986 and 2019. Tail feathers from females were collected annually, resulting in over 1000 feathers. Each feather served as an archive of local environmental conditions during molt, including the presence of metals, and their dietary ecology, proxied by stable isotopes of nitrogen (δ¹⁵N) and carbon (δ¹³C), as well as corticosterone levels (CORTf), the primary avian glucocorticoid and a measure of physiological stress. We analyzed feathers to examine how exposure to toxic metal(loid)s (Al, As, Cd, Hg, and Pb) and variability in dietary proxies modulate CORTf. Using structural equation modelling, we found that increased Al concentrations and δ¹⁵N values, linked directly to increased CORTf. In opposite, we found that increased Hg concentrations and δ¹³C related to decreased CORTf concentrations. δ¹⁵N was indirectly linked to CORTf through Al and Hg, while δ¹³C was indirectly linked to CORTf through Hg. This supports our hypothesis that metal exposure and dietary ecology may individually or jointly influence physiological stress. Notably, our results suggest that dietary ecology has the potential to mediate the impact of metals on CORTf, highlighting the importance of considering multiple variables, direct and indirect effects, when assessing stress in wildlife. In conclusion, feathers represent an excellent non-destructive biomonitoring strategy in avian wildlife, providing valuable insights not easily accessible using other methods. Further research is warranted to fully comprehend implications of alterations in CORTf on the tawny owl's health and fitness.