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Modulation of monoamine neurotransmitters in fighting fish Betta splendens exposed to waterborne phytoestrogens

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Abstract

Endogenous estrogens are known to affect the activity of monoamine neurotransmitters in vertebrate animals, but the effects of exogenous estrogens on neurotransmitters are relatively poorly understood. We exposed sexually mature male fighting fish Betta splendens to environmentally relevant and pharmacological doses of three phytoestrogens that are potential endocrine disruptors in wild fish populations: genistein, equol, and β-sitosterol. We also exposed fish to two doses of the endogenous estrogen 17β-estradiol, which we selected as a positive control because phytoestrogens are putative estrogen mimics. Our results were variable, but the effects were generally modest. Genistein increased dopamine levels in the forebrains of B. splendens at both environmentally relevant and pharmacological doses. The environmentally relevant dose of equol increased dopamine levels in B. splendens forebrains, and the pharmacological dose decreased norepinephrine (forebrain), dopamine (hindbrain), and serotonin (forebrain) levels. The environmentally relevant dose of β-sitosterol decreased norepinephrine and dopamine in the forebrain and hindbrain, respectively. Our results suggest that sources of environmental phytoestrogens, such as runoff or effluent from agricultural fields, wood pulp mills, and sewage treatment plants, have the potential to modulate neurotransmitter activity in free-living fishes in a way that could interfere with normal behavioral processes.

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Acknowledgments

We thank Lexi Brown, Maureen Manning, Kathy Nieves-Puigdoller, and Karina Zaveri for assistance in the laboratory. Mόnica Giusti and Dante Vargas at Ohio State University kindly performed the HPLC to validate our nominal genistein concentrations. Cynthia Bethea, Lexi Brown, Heather Patisaul, Brigitte Todd, and three anonymous reviewers provided helpful comments on earlier versions of this paper. Funding for this research was provided by the Webster Fund of the Department of Biology at Amherst College, the H. Axel Schupf ‘57 Fund for Intellectual Life at Amherst College, National Science Foundation grant IOS-0725186 to E.D.C. and National Institutes of Health COBRE grant P20 RR15567 to C.H.S.

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Authors and Affiliations

  1. Department of Biology, Amherst College, Amherst, MA, 01002, USA

    Ethan D. Clotfelter & Meredith M. McNitt

  2. Department of Biology, University of South Dakota, Vermillion, SD, 57069, USA

    Russ E. Carpenter & Cliff H. Summers

  3. Neuroscience Group, Division of Basic Biomedical Sciences, Sanford School of Medicine, University of South Dakota, Vermillion, SD, 57069, USA

    Cliff H. Summers

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  1. Ethan D. Clotfelter
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  2. Meredith M. McNitt
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Correspondence to Ethan D. Clotfelter.

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Clotfelter, E.D., McNitt, M.M., Carpenter, R.E. et al. Modulation of monoamine neurotransmitters in fighting fish Betta splendens exposed to waterborne phytoestrogens. Fish Physiol Biochem 36, 933–943 (2010). https://doi.org/10.1007/s10695-009-9370-2

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