Social status modulates the behavioral and physiological consequences of a chemical pollutant in animal groups

Abstract

The social environment (i.e., the suite of social interactions that occur among individuals, which can result in variation in social ranks) is a commonly overlooked aspect of biology when scientists evaluate the effects of chemical contaminants. The social environment, however, represents the arena in which individual-level performance shapes group- or population-level outcomes, and may therefore mediate many of the ultimate consequences of chemicals for wildlife. Here, we evaluated the role that the social environment plays in determining the consequences of pollutant exposure. We exposed groups of juvenile brown trout (Salmo trutta) to an emerging pharmaceutical pollutant that is commonly detected in freshwaters (the benzodiazepine, oxazepam), and allowed them to form dominance hierarchies. Exposure affected dominant and subordinate fish differently, causing fish to become less aggressive at high doses and subordinate fish to become more competitively successful at low doses. These perturbations had further consequences for growth, fin damage, and survival. Exposure also modulated physiological stress in the hierarchy, and social status itself affected how much oxazepam was absorbed in tissues - potentially creating a dynamic feedback loop that further influences the asymmetric effects of exposure on differing social statuses. Many effects followed a "U-shaped" dose-response, highlighting the importance of non-linear, low dose effects. Altogether, we show that social structure in animal groups can interact with and modulate the effects of an environmental contaminant. We underscore the need to account for an organism's natural ecological context, including their social environment, in future experiments and environmental risk assessments to predict the effects of chemical contaminants on wildlife.