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

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.

Exposure to an androgenic agricultural pollutant does not alter metabolic rate, behaviour, or morphology of tadpoles.

Globally, amphibian species are experiencing dramatic population declines, and many face the risk of imminent extinction. Endocrine-disrupting chemicals (EDCs) have been recognised as an underappreciated factor contributing to global amphibian declines. In this regard, the use of hormonal growth promotants in the livestock industry provides a direct pathway for EDCs to enter the environment-including the potent anabolic steroid 17ß-trenbolone. Emerging evidence suggests that 17ß-trenbolone can impact traits related to metabolism, somatic growth, and behaviour in non-target species. However, far less is known about possible effects of 17ß-trenbolone on anuran species, particularly during early life stages. Accordingly, in the present study we investigated the effects of 28-day exposure to 17ß-trenbolone (mean measured concentrations: 10 and 66 ng/L) on body size, body condition, metabolic rate, and anxiety-related behaviour of tadpoles (Limnodynastes tasmaniensis). Specifically, we measured rates of O2 consumption of individual tadpoles as a proxy for metabolic rate and quantified their swimming activity and their time spent in the upper half of the water column as indicators of anxiety-related behaviour. Counter to our predictions based on effects observed in other taxa, we detected no effect of 17ß-trenbolone on body size, metabolic rate, or behaviour of tadpoles; although, we did detect a subtle, but statistically significant decrease in body condition at the highest 17ß-trenbolone concentration. We hypothesise that 17ß-trenbolone may induce taxa-specific effects on metabolic function, growth, and anxiety-related behaviour, with anurans being less sensitive to disruption than fish, and encourage further cross-taxa investigation to test this hypothesis.

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.

Psychoactive pollution suppresses individual differences in fish behaviour.

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.