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. 2014 Jun:151:77-83.
doi: 10.1016/j.aquatox.2013.10.012. Epub 2013 Oct 16.

Environmental concentrations of the selective serotonin reuptake inhibitor fluoxetine impact specific behaviors involved in reproduction, feeding and predator avoidance in the fish Pimephales promelas (fathead minnow)

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Environmental concentrations of the selective serotonin reuptake inhibitor fluoxetine impact specific behaviors involved in reproduction, feeding and predator avoidance in the fish Pimephales promelas (fathead minnow)

Joel Weinberger 2nd et al. Aquat Toxicol. 2014 Jun.

Abstract

Pharmaceuticals and personal care products (PPCPs) have been found in surface waters worldwide, but little is understood of their effects on the wildlife that inhabit these waters. Fluoxetine (Prozac; Eli Lilly), a highly prescribed selective serotonin reuptake inhibitor (SSRI), is a commonly found PPCP in surface water. The purpose of this project was to determine if environmentally relevant concentrations of fluoxetine impact behavior that is important for population survival in native fish species, including reproduction, feeding and predator avoidance. Chronic 4-week exposures were conducted with doses ranging from 100 ng/L to 100 μg/L to cover a range of environmentally relevant concentrations up to higher concentrations comparable to other published studies with the same drug that have documented various physiological impacts. Pimephales promelas (fathead minnow), a species native to North America, was used as it conducts a range of specific mating behaviors and therefore serves as an excellent model of specific impacts on brain function. Fluoxetine concentrations as low as 1 μg/L, a concentration that has been found in many freshwater environments, were found to significantly impact mating behavior, specifically nest building and defending in male fish. Males were also found to display aggression, isolation, and repetitive behaviors at higher concentrations. Female mating behavior was largely unaffected. In addition, predator avoidance behaviors in males and females were also impacted at 1 μg/L. Feeding was impacted at 10 μg/L and in the highest exposure (100 μg/L), egg production was limited by deaths of females due to significant male aggressive behaviors in the first two weeks of exposure. Specific behavioral changes occurred at each concentration (most noticeably 1 μg/L and 100 μg/L) indicating a dose dependent effect that triggered different responses at lower exposures versus higher exposures or differential impacts of dose depending on brain region. Length of exposure also had an impact on aggressive behavior. Changes in hormone levels, indicating significant neuroendocrine changes, suggested as a mechanism of response in higher dose and acute studies, were not linked to changes in behaviors at the doses used in this study. This research provides detailed data on how exposures to fluoxetine impact specific fish behaviors and reproduction and that the effects are dose dependent.

Keywords: Fecundity; Mating; Neuroendocrine; Pharmaceuticals; Prozac; SSRI.

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Conflict of interest statement

Conflict of Interest

The authors have nothing to disclose.

Figures

Figure 1
Figure 1. Average amount of time male spent cleaning mating tile
The average amount of time males spent cleaning mating tile in 0, 0.1, 1, 10, or 100 μg/l fluoxetine exposures. Time spent cleaning was significantly different between control, 0.1 μg/l fluoxetine doses and 1 or 100 μg/l fluoxetine doses (Tukey HSD p < 0.05).
Figure 2
Figure 2. Average amount of time males spent under mating tile for each visit
The average amount of time males spent under mating tile for each visit during the observation period of fathead minnows while exposed to 0, 0.1, 1, 10, or 100 μg/l of fluoxetine are shown. The amount of time males spent under the tile for each visit was significantly different between 100 μg/l fluoxetine and other doses (Tukey HSD p < 0.05).
Figure 3
Figure 3. Average amount male visited mating mating tile
The average amount males visited the mating tile to clean, mate with female, or swim under tile during observations while exposed to 0, 0.1, 1, 10, or 100 μg/l fluoxetine. Number of exits was significantly different between control and 1 μg/l fluoxetine doses and the 100 μg/l fluoxetine dose (Tukey HSD p<0.05).
Figure 4
Figure 4. Average total amount of eggs laid impacted by highest fluoxetine exposure
The average total amount of eggs laid by all pairs during exposure to 0, 0.1, 1, 10, or 100 μg/L fluoxetine. Fluoxetine dose of 100 μg/l was significant to all other doses (Tukey HSD p < 0.05).
Figure 5
Figure 5. Average Time To Eat Prey Items Increases with Fluoxetine Exposure
Fish exposed to 1, 10 and 100 μg/L took longer to eat prey when presented 10 Daphnia than 0 and 0.1 μg/L treatments (Tukey HSD p < 0.05).
Figure 6
Figure 6. Distance Minnow Swam When Presented With a Model Predator Fish exposed to
Distance fathead minnows swam away when presented with a large spot representing the approach of a predator. Fish exposed to 10 and 100 μg/L fluoxetine moved a smaller distance when compared with other treatments (Tukey HSD p < 0.05).

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