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Ecotoxicology and Human Environmental Health
Antidepressants in surface waters: fluoxetine influences mosquitofish anxiety-related behavior at environmentally relevant levels Jake Martin, Michael G Bertram, Minna Saaristo, Jack B Fursdon, Stephanie L Hannington, Bryan W Brooks, S. Rebekah Burket, Rachel Mole, Nicholas D.S Deal, and Bob B.M. Wong Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.9b00944 • Publication Date (Web): 29 Apr 2019 Downloaded from http://pubs.acs.org on April 30, 2019
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Fluoxetine exposure 28-day
*Scototaxis
0.2431 mm
0 ng/L
+
*Shoaling
Disrupted Sociability
♀ ♂
Gambusia holbrooki
0.2301
Unaffected Tissue concentrations Tissue concentration
61 ng/L 352 ng/L
Morphology
Anxiety behavior
Unaffected ACS Paragon Plus Environment
Body weight
Biomass-dependent
Environmental Science & Technology
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Antidepressants in surface waters: fluoxetine
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influences mosquitofish anxiety-related
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behavior at environmentally relevant levels
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Jake M. Martin 1,* Michael G. Bertram 1, Minna Saaristo 1 , Jack B. Fursdon 1, Stephanie L.
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Hannington 1, Bryan W. Brooks 2,3, S. Rebekah Burket 2, Rachel A. Mole 2,
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Nicholas D.S. Deal 1, Bob B.M. Wong 1
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1 School
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2 Department
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of Biological Sciences, Monash University, Victoria, Australia. of Environmental Science, Baylor University, Texas, United States.
3 School
of Environment, Jinan University, Guangzhou, China.
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* Corresponding author at:
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School of Biological Sciences, Monash University,
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Melbourne, Victoria 3800, Australia
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E-mail address:
[email protected] (J.M. Martin).
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Abstract
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Pharmaceutical contamination is an increasing problem globally. In this regard, the
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selective serotonin reuptake inhibitors (SSRIs)—a group of antidepressants—are
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particularly concerning. By disrupting the serotonergic system, SSRIs have the
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potential to affect ecologically important behaviors in exposed wildlife. Despite this,
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the nature and magnitude of behavioral perturbations resulting from environmentally
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relevant SSRI exposure among species is poorly understood. Accordingly, we
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investigated effects of two field-realistic levels of the SSRI fluoxetine (61 and 352 ng/L)
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on sociability and anxiety-related behaviors in eastern mosquitofish (Gambusia
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holbrooki) for 28 days. Additionally, we measured whole-body tissue concentrations
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of fluoxetine and norfluoxetine. We found that fluoxetine altered anxiety-related 2 ACS Paragon Plus Environment
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behavior but not sociability. Specifically, female fish showed reduced anxiety-related
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behavior at the lower treatment level, while males showed an increase at the higher
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treatment level. In addition, we report a biomass-dependent and sex-specific
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accumulation of fluoxetine and norfluoxetine, with smaller fish showing higher relative
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tissue concentrations, and this relationship being more pronounced in males. Our
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study provides evidence for nonmonotonic and sex-specific effects of fluoxetine
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exposure at field-realistic concentrations. More broadly, our study demonstrated that
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neuroactive pharmaceuticals, such as fluoxetine, can affect aquatic life by causing
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subtle but important shifts in ecologically relevant behaviors.
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Keywords 3 ACS Paragon Plus Environment
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Behavioral ecotoxicology; Bioaccumulation; Fish; Scototaxis; Sex-dependent effect;
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sociability; SSRI.
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1. Introduction
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Pharmaceutical contamination of the environment is an increasing global problem.1,2
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To date, over 600 different pharmaceuticals have been detected in aquatic
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ecosystems and wildlife tissues around the world.3 Further, the release of
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pharmaceuticals into the environment is likely to escalate due to growing urbanization,
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and a continuing increase in production and diversification of pharmaceutical
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products.4 Indeed, recent analyses suggest the growth in production of synthetic
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chemicals, including pharmaceuticals, is equal to or may exceed most other
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recognized drivers of global change (e.g. climate change, habitat loss, rising
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atmospheric CO2).4 Such chemical stressors may result in subtle ecological impacts,
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including modulation of ecologically relevant behaviors critical to reproduction and
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survival.
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Among emerging environmental contaminants, the selective serotonin reuptake
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inhibitors (SSRIs) are of increasing concerning. This is because SSRIs are amongst 4 ACS Paragon Plus Environment
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the world’s most commonly prescribed antidepressants and are the most frequently
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detected in the environment.5,6 This group of drugs has been found in surface and
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ground waters globally, typically between
