Unravelling the intricate effects of metal contamination on pathogen infection risk and fish health

Metal contamination and pathogens often co-occur in freshwater ecosystems, yet their combined effects on wildlife health remain poorly understood. We investigated whether metal contamination modulates disease risk and fish health in brown trout (Salmo trutta, Linnaeus, 1758) exposed to the pathogen Tetracapsuloides bryosalmonae (Canning, 1999), responsible for the Proliferative Kidney Disease (PKD). We sampled 40 wild trout populations along gradients of metal contamination (copper, zinc, arsenic, selenium, cadmium, lead) and pathogen infection in French Pyrenean rivers. Using Structural Equation Modelling, we tested how metal contamination was linked to pathogen pressure in the environment, pathogen load in fish (resistance), PKD symptoms (tolerance) and fish health biomarkers. We show that rivers with higher metal concentrations were negatively associated with bryozoan occurrence (the pathogen's final host), which was in turn associated with reduced pathogen pressure (pathogen spores in the water). In addition, metal concentration in fish tissue was associated with altered health biomarkers and pathogen load, depending on the metal considered. First, higher selenium concentrations in fish tissues were associated with increased pathogen load, suggesting low resistance to the pathogen. Second, higher arsenic concentrations in fish tissues were linked to increased PKD symptoms (kidney swelling and anaemia), suggesting reduced tolerance to the pathogen. Third, higher concentrations of cadmium in fish tissues were associated with reduced immune ratios, while copper was positively linked to genotoxic damage and energy depletion, resulting in lower body condition. In contrast, no clear relationship was observed between lead and fish health. Overall, our findings suggest that metal contamination could affect disease risk through direct effects on pathogen pressure in the environment, and through indirect effects on fish resistance/tolerance to the pathogen through metal-specific physiological pathways. By simultaneously considering pathogen pressure and multiple health biomarkers under natural conditions, this study highlights how co-occurring stressors could shape fish-pathogen interactions.