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

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

doi:10.1093/beheco/arad065

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

Behav Ecol. 2023 Aug 14;34(6):969-978. doi: 10.1093/beheco/arad065. eCollection 2023 Nov-Dec.

Authors

Giovanni Polverino^{1

2}, Upama Aich¹, Jack A Brand¹, Michael G Bertram³, Jake M Martin^{3

4}, Hung Tan¹, Vrishin R Soman⁵, Rachel T Mason^{1

6}, Bob B M Wong¹

Affiliations

¹ School of Biological Sciences, Monash University, 25 Rainforest Walk, Clayton, 3800, Victoria, Australia.
² Department of Ecological and Biological Sciences, University of Tuscia, L.go dell'Università snc, Viterbo, 01100, Italy.
³ Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, SE-907 36, Umeå,Sweden.
⁴ Department of Zoology, Stockholm University, Svante Arrhenius väg 18b114 18, Stockholm, Sweden.
⁵ Department of Mechanical and Aerospace Engineering, New York University , 370 Jay Street, Brooklyn, 11201, NY, USA.
⁶ School of Life and Environmental Sciences, Deakin University, 221 Burwood Highway, Burwood, 3125, Victoria, Australia.

Abstract

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.