Psychoactive pollution suppresses individual differences in fish behaviour

Abstract

Environmental contamination by pharmaceuticals is global, substantially altering crucial behaviours in animals and impacting on their reproduction and survival. A key question is whether the consequences of these pollutants extend beyond mean behavioural changes, restraining differences in behaviour between individuals. In a controlled, two-year, multigenerational experiment with independent mesocosm populations, we exposed guppies ( Poecilia reticulata ) to environmentally realistic levels of the ubiquitous pollutant fluoxetine (Prozac). Fish (unexposed: n = 59, low fluoxetine: n = 57, high fluoxetine: n = 58) were repeatedly assayed on four separate occasions for activity and risk-taking behaviour. Fluoxetine homogenized individuals' activity, with individual variation in populations exposed to even low concentrations falling to less than half that in unexposed populations. To understand the proximate mechanism underlying these changes, we tested the relative contribution of variation within and between individuals to the overall decline in individual variation. We found strong evidence that fluoxetine erodes variation in activity between but not within individuals, revealing the hidden consequences of a ubiquitous contaminant on phenotypic variation in fish—likely to impair adaptive potential to environmental change.

Fluoxetine results in misleading conclusions on fish behavior

“…Confirmation of our theory can be found in a recent Polverino et al. (2021) publication. The authors found strong evidence that fluoxetine impairs adaptive potential to environmental change in fishes.…”

Warmer temperatures limit the effects of antidepressant pollution on life-history traits

“…The target molecule of fluoxetine (serotonin transporter, 5-HTT) is present in a wide variety of taxa [14], which gives fluoxetine the potential to affect non-target organisms. In fact, studies have shown that fluoxetine exposure can cause adverse effects in a range of aquatic organisms, including reduced fecundity in snails [15], impaired development in tadpoles [16] and disturbed behaviour in fish [17–19]. Few studies, however, have examined the impacts on life-history traits at field-relevant concentrations, which is surprising considering that changes in these traits are expected to have dire fitness and evolutionary consequences [7,20,21].…”

Frontiers in quantifying wildlife behavioural responses to chemical pollution

“…Given that only a relatively small number of recent studies have examined how chemical stressors alter aspects of behavioural variation (e.g. Tüzün et al ., 2017; Polverino et al ., 2021), or how consistent individual differences affect behavioural responses to chemical stressors (Nanninga, Scott & Manica, 2020), the integration of behavioural ecotoxicology and consistent individual variation is clearly an important direction for future study (see Montiglio & Royauté, 2014).…”

“…Indeed, recent work embracing these innovations has revealed effects of pollutants on behavioural processes that were previously not possible to capture using conventional approaches. These range from neurotoxic insecticide‐induced migration delays in songbirds (Eng, Stutchbury & Morrissey, 2019) to the breakdown of behavioural diversity in fish populations exposed to pharmaceutical pollution (Polverino et al ., 2021).…”