Antidepressant pollution disrupts reproduction in fish

Guest post by Michael Bertram, Student Blog Contest Series 

Have you ever wondered what happens to medicines after we take them? Are they completely absorbed by our bodies? The answer is ‘no’. Pharmaceuticals are often incompletely metabolised after ingestion and can eventually make their way into the environment. In fact, excretion by human patients is a major source of the over 600 different kinds of pharmaceutical substances that have now been detected in the environment worldwide, across 71 countries and all continents. 

Mosquitofish were used as a model to test impacts of pharmaceutical pollution. Photo by Andrew Kahn.

What’s more, pharmaceutical pollution is expected to increase in the future. This is because the use of medications by humans is escalating globally, with the number of pharmaceutical doses dispensed per annum being predicted to reach 4.5 trillion by 2020, an increase of 24% from 2015 levels.

So, given that pharmaceuticals are typically designed to have biological effects at low doses, could their presence in the environment potentially be affecting ecological and evolutionary processes in wildlife? To address this question, we conducted new research, published in Environmental Pollution, investigating impacts of exposure of fish to one of the world’s most common pharmaceutical pollutants, fluoxetine (marketed as Prozac).

 

 

More than 600 different pharmaceutical substances have now been detected in the environment. Photo by Gatis Gribusts.

Fish on drugs

After human patients ingest and excrete fluoxetine, this antidepressant drug makes its way into aquatic habitats mainly due to inadequate removal during wastewater treatment processes. Because fluoxetine is among the most commonly prescribed antidepressants globally, it has repeatedly been detected in aquatic environments around the world. Indeed, recent research investigating pharmaceutical concentrations in Sydney harbour in Australia revealed that levels of fluoxetine contamination were second only to paracetamol.

Previous research has demonstrated that fluoxetine exposure can cause a range of adverse effects in aquatic species, including disrupting development and reproduction, and altering morphological and physiological traits.

What’s more, given that fluoxetine is prescribed to treat psychiatric disorders in humans, recent research has focused on its potential to influence behaviour in wildlife. This work has revealed that exposure to fluoxetine can, for example, impair learning and memory retention in cuttlefish and reduce antipredator behaviour in guppies.

Despite these new findings, we currently know relatively little about how fluoxetine exposure at environmentally realistic levels might influence reproductive behaviour in wildlife, as is also true for pharmaceutical contaminants more generally. This is concerning given the fundamental role of reproductive processes in the ecology and evolution of populations and species. So, we conducted a series of experiments testing impacts of fluoxetine exposure on reproductive processes in male Eastern mosquitofish.

Male fish were first exposed to fluoxetine for 30 days at two field-realistic levels (‘low’ and ‘high’) using large-scale aquarium systems, before being assessed for mating behaviour, as well as sperm quality and quantity. These tests revealed, for the first time, that exposure to fluoxetine at levels consistent with those reported in the environment can disrupt both male reproductive behaviour and sperm production in fish.

In one-on-one mating trials, males in the high-fluoxetine treatment performed more frequent mating behaviour towards females than did unexposed males. Interestingly, however, male reproductive behaviour was not disrupted by fluoxetine exposure when in the presence of a rival male, suggesting interacting effects of fluoxetine exposure and male competition. Further, males exposed to fluoxetine at both the low and high levels were found to have higher sperm counts relative to unexposed males, while sperm performance was not significantly affected.

 

Computer-assisted sperm analysis software was used to assess sperm performance (each cell’s path is represented with a coloured line). Photo by Michael Bertram.

From the lab to the field

How are fluoxetine-induced changes in male reproductive behaviour seen in the lab expected to manifest in wild fish populations? The answer boils down to one key fact: altered behaviours, especially mating behaviour, can have drastic implications for the fitness of individuals, as well as ecosystem dynamics and evolutionary processes. This is because the ability of animals to appropriately perform reproductive behaviours plays a crucial role in determining which individuals can successfully reproduce.

Given that males in the high-fluoxetine exposure treatment performed increased mating behaviour towards females, and were also found to have increased sperm counts, this would suggest that, in nature, males inhabiting contaminated habitats may be more reproductively successful. However, given the complexity of natural systems, this possibility requires further investigation. For example, in mosquitofish, females have been shown to actively avoid males performing excessive mating behaviour, meaning that any potential increase in reproductive fitness in contaminated males will likely depend on their ability to appropriately adjust their behaviour to suit their environment.

Our findings highlight the potential for widespread pharmaceutical pollutants to disrupt key traits and behaviours in wildlife at exposure concentrations reflecting those present in the environment. Given the increasing pressure on wildlife and ecosystems from chemical pollution—including contaminants of emerging concern, such as pharmaceuticals—this research demonstrates the importance of considering ecologically meaningful endpoints in assessing the risks posed by these pollutants.

Literature cited

• ‘over 600 different pharmaceutical substances have now been detected’ — http://rstb.royalsocietypublishing.org/content/369/1656/20130587
• ‘across 71 countries spanning all continents’ — https://setac.onlinelibrary.wiley.com/doi/full/10.1002/etc.3339
• ‘predicted to reach 4.5 trillion by 2020, an increase of 24% from 2015 levels’ — https://www.iqvia.com/-/media/iqvia/pdfs/institute-reports/global-medicines-use-in-2020.pdf?la=uk-ua&hash=968B71C0B0769A179F3A56E331C62754EEF74752
• ‘Environmental Pollution’ — https://www.sciencedirect.com/science/article/pii/S026974911734856X?via%3Dihub
• ‘recent research’ — https://www.sciencedirect.com/science/article/pii/S0025326X15004051
• ‘development’ — https://link.springer.com/article/10.1007%2Fs00244-007-9018-0
• ‘reproduction’ — https://www.sciencedirect.com/science/article/pii/S0166445X09001404?via%3Dihub
• ‘altering morphological and physiological traits’ — https://www.sciencedirect.com/science/article/pii/S0045653515006529?via%3Dihub
• ‘impair learning and memory retention in the common cuttlefish’ —
• https://www.sciencedirect.com/science/article/pii/S0166445X13000362?via%3Dihub
• ‘reduce antipredator behaviour in guppies’ — https://www.sciencedirect.com/science/article/pii/S0045653515006529
• ‘can have drastic implications for organismal fitness, as well as ecosystem dynamics and evolutionary processes’ — https://academic.oup.com/beheco/article/26/3/665/233718
• ‘females have been shown to actively avoid males performing excessive copulation attempts’ — https://www.sciencedirect.com/science/article/pii/S000334720392118X

About the author

Michael Bertram is a Ph.D. candidate studying behavioural ecology and ecotoxicology at the School of Biological Sciences, Monash University, Australia.