Context is Key: Social Environment Mediates the Impacts of a Psychoactive Pollutant on Shoaling Behavior in Fish

Behavior-modifying drugs, such as antidepressants, are increasingly being detected in waterways and aquatic wildlife around the globe. Typically, behavioral effects of these contaminants are assessed using animals tested in social isolation. However, for group-living species, effects seen in isolation may not reflect those occurring in realistic social settings. Furthermore, interactions between chemical pollution and other stressors, such as predation risk, are seldom considered. This is true even though animals in the wild are rarely, if ever, confronted by chemical pollution as a single stressor. Here, in a 2 year multigenerational experiment, we tested for effects of the antidepressant fluoxetine (measured concentrations [±SD]: 42.27 ± 36.14 and 359.06 ± 262.65 ng/L) on shoaling behavior in guppies (Poecilia reticulata) across different social contexts and under varying levels of perceived predation risk. Shoaling propensity and shoal choice (choice of groups with different densities) were assessed in a Y-maze under the presence of a predatory or nonpredatory heterospecific, with guppies tested individually and in male-female pairs. When tested individually, no effect of fluoxetine was seen on shoaling behavior. However, in paired trials, high-fluoxetine-exposed fish exhibited a significantly greater shoaling propensity. Hence, effects of fluoxetine were mediated by social context, highlighting the importance of this fundamental but rarely considered factor when evaluating impacts of environmental pollution.