Intraspecific variability of responses to combined metal contamination and immune challenge among wild fish populations

Wild organisms are increasingly exposed to multiple anthropogenic and natural stressors that can interact in complex ways and lead to unexpected effects. In aquatic ecosystems, contamination by trace metals has deleterious effects on fish health and commonly co-occurs with pathogens, which affect similar physiological and behavioral traits. However, the combined effects of metal contamination and parasitism are still poorly known. In addition, the sensitivity to multiple stressors could be highly variable among different fish populations depending on their evolutionary history, but this intraspecific variability is rarely taken into account in existing ecotoxicological studies. Here, we investigated i) the interactive effects of metal contamination (i.e., realistic mixture of Cd, Cu and Zn) and immune challenge mimicking a parasite attack on fish health across biological levels. In addition, we compared ii) the physiological and behavioral responses among five populations of gudgeon fish (Gobio occitaniae) having evolved along a gradient of metal contamination. Results show that single stressors exposure resulted in an increase of immune defenses and oxidative stress at the expense of body mass (contamination) or fish swimming activity (immune challenge). Multiple stressors had fewer interactive effects than expected, especially on physiological traits, but mainly resulted in antagonistic effects on fish swimming activity. Indeed, the immune challenge modified or inhibited the effects of contamination on fish behavior in most populations, suggesting that multiple stressors could reduce behavioral plasticity. Interestingly, the effects of stressors were highly variable among populations, with lower deleterious effects of metal contamination in populations from highly contaminated environments, although the underlying evolutionary mechanisms remain to be investigated. This study highlights the importance of considering multiple stressors effects and intraspecific variability of sensitivity to refine our ability to predict the effects of environmental contaminants on aquatic wildlife.