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Research article - Peer-reviewed, 2023

Sex-specific effects of psychoactive pollution on behavioral individuality and plasticity in fish

Polverino, Giovanni; Aich, Upama; Brand, Jack A.; Bertram, Michael G.; Martin, Jake M.; Tan, Hung; Soman, Vrishin R.; Mason, Rachel T.; Wong, Bob B. M.

Abstract

Lay Summary Prozac is present in freshwater systems across the globe as the pharmaceutical contaminant fluoxetine. The effect of fluoxetine on aquatic species' behavioral variability is not yet clear. We show that male guppies become more similar to each other after exposure to fluoxetine, and females become less flexible in their behavior. These sex-specific differences in response to fluoxetine can have a meaningful impact on their ability to survive in a changing world.The global rise of pharmaceutical contaminants in the aquatic environment poses a serious threat to ecological and evolutionary processes. Studies have traditionally focused on the collateral (average) effects of psychoactive pollutants on ecologically relevant behaviors of wildlife, often neglecting effects among and within individuals, and whether they differ between males and females. We tested whether psychoactive pollutants have sex-specific effects on behavioral individuality and plasticity in guppies (Poecilia reticulata), a freshwater species that inhabits contaminated waterways in the wild. Fish were exposed to fluoxetine (Prozac) for 2 years across multiple generations before their activity and stress-related behavior were repeatedly assayed. Using a Bayesian statistical approach that partitions the effects among and within individuals, we found that males-but not females-in fluoxetine-exposed populations differed less from each other in their behavior (lower behavioral individuality) than unexposed males. In sharp contrast, effects on behavioral plasticity were observed in females-but not in males-whereby exposure to even low levels of fluoxetine resulted in a substantial decrease (activity) and increase (freezing behavior) in the behavioral plasticity of females. Our evidence reveals that psychoactive pollution has sex-specific effects on the individual behavior of fish, suggesting that males and females might not be equally vulnerable to global pollutants.

Keywords

animal personality; contamination; ecotoxicology; environmental change; fluoxetine; pharmaceutical pollution; sex differences; sexual dimorphism

Published in

Behavioral Ecology
2023, Volume: 34, number: 6, pages: 969-978