Heavy metals (HM) of anthropogenic origin are considered to be major environmental toxicants with deleterious effects on virtually all life forms. In particular, the accumulation in tissues of non-essential elements, such as cadmium or lead, is toxic even at low levels and is known to have serious impacts on wildlife health. Actually, such contaminants might represent new selective pressures in natural systems. However, the underlying physiological mechanisms linking HM to individual health are not fully elucidated and remain to be studied in the wild. Using an ungulate as study model, we tested whether high HM concentrations were associated with a compromised oxidative balance (accumulation of oxidative damages and/or low antioxidant levels) and a higher stress response (baseline glucocorticoids levels). We also examined whether individual (age, sex, body mass) and environmental (study site) characteristics affected the link between HM and each biomarker.

We collected hair, feces, and blood samples from 429 wild roe deer captured over four years in two French populations with contrasted environmental conditions (Trois-Fontaines and Chizé). We measured hair concentrations of nine heavy metals, plasma levels of five markers of oxidative balance, and fecal glucocorticoid metabolites (FGMs). Using a multivariate analysis approach, and linear mixed-effects models, we showed either an increase or a decrease in antioxidant defenses, an increase in oxidative damages, and an increase in FGMs with increasing HM concentrations. This study therefore suggests that exposure to HM can disrupt the oxidative balance and promote baseline glucocorticoids elevation, with expected implications for individual performance and ultimately population viability. Results also reveal physiological sensitivities according to individual and/or environmental characteristics, since observed patterns differed according to population, age and body mass. More specifically, we highlight different oxidative stress patterns and stress coping strategies at the individual and population level.

These results allow to better understand the mechanisms by which the health of wild populations can be affected by HM contamination. This raises the question of the implications of ongoing anthropogenic pollution in natural habitats as an emerging evolutionary pressure for global animal populations health.