Skip to main content

Fluoxetine exposure impacts boldness in female Siamese fighting fish, Betta splendens

Abstract

The present study examined the effects of the selective serotonin reuptake inhibitor, fluoxetine, on the behavior of female Siamese fighting fish, Betta splendens, in three different boldness assays (Empty Tank, Novel Environment, Social Tendency). When females were unexposed to fluoxetine, boldness was consistent within a context and correlated across assays. Fluoxetine exposure affected behavior within and among individuals on multiple levels. Exposure reduced overall boldness levels, made females behave in a less consistent manner, and significantly reduced correlations over time and across contexts. Fluoxetine exerted its effects on female Betta splendens behavior in a dose-dependent fashion and these effects persisted even after females were housed in clean water. If fluoxetine exposure impacts behaviors such as exploration that are necessary to an individual’s success, this may yield evolutionary consequences. In conclusion, the results show that fluoxetine exposure alters behavior beyond the level of overall response and highlights the importance of studying the behavioral effects of inadvertent pharmaceutical exposure in multiple contexts and with different dosing regimes.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  • Arnold KE, Boxall ABA, Brown AR, Cuthbert RJ, Gaw S, Hutchinson TH et al (2013) Assessing the exposure risk and impacts of pharmaceuticals in the environment on individuals and ecosystems. Biol Lett 9:20130492

    Article  Google Scholar 

  • Asendorf JB (1990) The measurement of individual consistency. Methodika 4:1–23

    Google Scholar 

  • Barnes KK, Kolpin DW, Furlong ET, Zaugg SD, Meyer MT, Barber LB (2008) A national reconnaissance of pharmaceuticals and other organic wastewater contaminants in the United States. 1. Groundwater. Sci Tot Environ 402:192–200

    Article  CAS  Google Scholar 

  • Barry MJ (2013) Effects of fluoxetine on swimming and behavioral responses of the Arabian killifish. Ecotoxicology 22:425–432

    Article  CAS  Google Scholar 

  • Bell AM (2007) Future directions in behavioral syndromes research. Proc R Soc Lond B 275:755–761

    Article  Google Scholar 

  • Blair BD, Crago JP, Hedman CJ, Klaper R (2013) Pharmaceutical and personal care products found in the great lakes above concentrations of environmental concern. Chemosphere 93:2116–2123

    Article  CAS  Google Scholar 

  • Boake CRB (1989) Repeatability: its role in evolutionary studies of mating behavior. Evol Ecol 3:173–182

    Article  Google Scholar 

  • Briffa M, Sneddon LU, Wilson AJ (2015) Animal personality as a cause and consequence of contest behavior. Biol Lett 11:20141007

    Article  Google Scholar 

  • Brooks BW (2014) Fish on Prozac (and Zoloft): ten years later. Aquat Toxicol 151:61–67

    Article  CAS  Google Scholar 

  • Budaev SV (2010) Using principal components and factor analysis in animal behavior research: caveats and guidelines. Ethology 116:472–480

    Article  Google Scholar 

  • Clements S, Schreck CB (2007) Chronic administration of fluoxetine alters locomotor behavior, but does not potentiate the locomotor stimulating effects of CRH in juvenile Chinook salmon (Oncorhynchus tshawytscha). Comp Biochem Physiol A 147:43–49

    Article  CAS  Google Scholar 

  • Clotfelter ED, Rodriguez AC (2006) Behavioral changes in fish exposed to phytoestrogens. Environ Poll 144:833–839

    Article  CAS  Google Scholar 

  • Cockrem J (2007) Stress, corticosterone responses and avian personalities. J Ornithol 148:169–178

    Article  Google Scholar 

  • Coppens CM, de Boer SF, Koolhaas JM (2010) Coping styles and behavioral flexibility: towards underlying mechanisms. Phil Trans Lond B 365:4021–4028

    Article  Google Scholar 

  • De Lange HJ, Noordoven R, Murk AJ, Lürling M, Peeters ETHM (2006) Behavioral responses of Gammarus pulex (Crustacea, Amphipoda) to low concentrations of pharmaceuticals. Aquat Toxicol 78:209–216

    Article  CAS  Google Scholar 

  • De Pedro N, Pinillos ML, Valenciano AI, Alonso-Bedate M, Delgado MJ (1998) Inhibitory effect of serotonin on feeding behavior in goldfish: involvement of CRF. Peptides 19:505–511

    Article  Google Scholar 

  • Decker RA, Griffen BD (2012) Correlating context-specific boldness and physiological condition of female sand fiddler crabs (Uca pugilator). J Ethol 30:403–412

    Article  Google Scholar 

  • Di Poi C, Bidel F, Dickel L, Bellanger C (2014) Cryptic and biochemical responses of young cuttlefish Sepia officinalis exposed to environmentally relevant concentrations of fluoxetine. Aquat Toxicol 151:36–45

    Article  CAS  Google Scholar 

  • Dingemanse NJ, Reale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184

    Article  Google Scholar 

  • Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioral syndromes. Tren Ecol Evol 23:502–510

    Article  Google Scholar 

  • Dzieweczynski TL, Hebert OL (2013) The effects of short-term exposure to an endocrine disrupter on behavioral consistency in juvenile and adult male Siamese fighting fish. Arch Environ Contamin Toxicol 64:316–326

    Article  CAS  Google Scholar 

  • Dzieweczynski TL, Campbell BA, Marks JM, Logan B (2014) Acute exposure to 17α-ethinylestradiol alters boldness behavioral syndrome in female Siamese fighting fish. Horm Behav 66:577–584

    Article  CAS  Google Scholar 

  • Egan RJ, Bergner CL, Hart PC, Cachat JM, Canavello PR, Elegante MF et al (2009) Understanding behavioural and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res 205:38–44

    Article  CAS  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Pearson Prentice Hall, Harlow

    Google Scholar 

  • Fent K, Westron AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76:122–159

    Article  CAS  Google Scholar 

  • Gaworecki KM, Klaine SJ (2008) Behavioral and biochemical responses of hybrid striped bass during and after fluoxetine exposure. Aquat Toxicol 88:207–213

    Article  CAS  Google Scholar 

  • Griffin LD, Mellon SH (1999) Selective serotonin reuptake inhibitors directly alter activity of neurosteroidogenic enzymes. Proc Natl Acad Sci USA 96:13512–13517

    Article  CAS  Google Scholar 

  • Guler Y, Ford AT (2010) Anti-depressants make amphipods see the light. Aquat Toxicol 99:397–404

    Article  CAS  Google Scholar 

  • Hazelton PD, Du B, Haddad SP, Fritts AK, Chambliss CK, Brooks BW, Bringolf RB (2014) Chronic fluoxetine exposure alters movement and burrowing in adult freshwater mussels. Aquat Toxicol 151:27–35

    Article  CAS  Google Scholar 

  • Hebert OL, Lavin LE, Marks JM, Dzieweczynski TL (2014) The effects of 17α-ethinylestradiol on boldness and its relationship to decision-making in male Siamese fighting fish. Anim Behav 87:203–212

    Article  Google Scholar 

  • Invernizzi R, Bramante M, Samanin R (1996) Role of 5-HT1A receptors in the effects of acute and chronic fluoxetine on extracellular serotonin in the frontal cortex. Pharmacol Biochem Behav 54:143–147

    Article  CAS  Google Scholar 

  • Jones KA, Godin JGJ (2010) Are fast explorers slow reactors? Linking personality type and anti-predator behavior. Proc R Soc B 277:625–632

    Article  Google Scholar 

  • Khan IA, Thomas P (1992) Stimulatory effects of serotonin on maturational gonadotropin release in the Atlantic croaker Micropogonias undulates. Gen Comp Endocrinol 88:388–396

    Article  CAS  Google Scholar 

  • Kohlert JG, Mangan BP, Kodra C, Drako L, Long E, Simpson H (2012) Decreased aggressive and locomotor behaviors in Betta splendens after exposure to fluoxetine. Psychol Rep 110:51–62

    Article  Google Scholar 

  • Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999–2000: a national reconnaissance. Environ Sci Tech 36:1202–1211

    Article  CAS  Google Scholar 

  • Kostich MS, Lazorachak JM (2008) Risks to aquatic organisms posed by human pharmaceutical use. Sci Tot Environ 389:329–339

    Article  CAS  Google Scholar 

  • Kurvers R, Prins HHT, van Wieren SE, van Oers C, Nolet BA, Ydenberg RC (2010) The effect of personality on social foraging: shy barnacle geese scrounge more. Proc R Soc B 277:601–608

    Article  Google Scholar 

  • Lister A, Regan C, Van Zwol J, Van Der Kraak G (2009) Inhibition of egg production in zebrafish by fluoxetine and municipal effluents: a mechanistic evaluation. Aquat Toxicol 95:320–329

    Article  CAS  Google Scholar 

  • Lynn SE, Egar JM, Walker BG, Sperry TS, Ramenofsky M (2007) Fish on Prozac: a simple, noninvasive physiology laboratory investigating the mechanisms of aggressive behavior in Betta splendens. Adv Physiol Ed 31:353–363

    Google Scholar 

  • Mennigen JA, Crump K, Xiong H, Zhao E, Popesku P, Anisman H, Xiz X, Trudeau VL (2008) The effects of fluoxetine on the reproductive axis of female goldfish (Carrasius auratus). Physiol Gen 35:273–282

    Article  CAS  Google Scholar 

  • Metcalfe CD, Chu S, Judt C, Li H, Oakes KD, Servos MR, Andrews DM (2003) Antidepressants and their metabolites in municipal wastewater, and downstream exposure in an urban watershed. Environ Sci Chem 29:79–89

    Google Scholar 

  • Muneoka K, Shirayama Y, Takigawa M, Shioda S (2009) Brain region-specific effects of short-term treatment with duloxetine, venlafaxine milnacipran and sertaline on monoamine metabolism in rats. Neurochem Res 34:542–555

    Article  CAS  Google Scholar 

  • Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    Google Scholar 

  • Olsén KH, Ask K, Olsén H, Porsch-Hällström I, Hallgren S (2014) Effects of the SSRI citalopram on behaviors connected to stress and reproduction in Endler guppy, Poecilia wingei. Aquat Toxicol 148:113–121

    Article  CAS  Google Scholar 

  • Oswald ME, Drew RE, Racine M, Murdoch GK, Robison BD (2013) Is behavioral variation along the bold-shy continuum associated with variation in the stress axis in zebrafish? Physiol Biochem Zool 85:718–728

    Article  Google Scholar 

  • Perreault HAN, Semsar K, Godwin J (2003) Fluoxetine treatment decreases territorial aggression in a coral reef fish. Physiol Behav 79:719–724

    Article  CAS  Google Scholar 

  • Prieto MJ, Gutierrez HC, Arévalo RA, Chiaramoni NS, del Valle Alonso S (2012) Effect of risperodone and fluoxetine on the movement and neurochemical changes of zebrafish. J Med Chem 2:129–138

    CAS  Google Scholar 

  • Schuett W, Dall SRX (2009) Sex differences, social context and personality in zebra finches, Taeniopygia guttata. Anim Behav 77:1041–1050

    Article  Google Scholar 

  • Sebastine IM, Wakeman RJ (2003) Consumption and environmental hazards of pharmaceutical substances in the UK. Proc Saf Environ Protect 81:229–235

    Article  CAS  Google Scholar 

  • Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Quart Rev Biol 79:241–277

    Article  Google Scholar 

  • Sinn DL, Apiolaza LA, Moltschaniwskyj NA (2006) Heritability and fitness-related consequences of squid personality traits. J Evol Biol 19:1437–1447

    Article  CAS  Google Scholar 

  • van Oers K, Klunder M, Drent PJ (2005) Context dependence of personalities: risk-taking behavior in a social and nonsocial situation. Behav Ecol 16:716–723

    Article  Google Scholar 

  • Weinberger J III, Klaper R (2014) 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). Aquat Toxicol 151:77–83

    Article  CAS  Google Scholar 

  • Wilson DS, Clark AB, Coleman K, Dearstyne T (1994) Shyness and boldness in humans and other animals. Tren Ecol Evol 9:442–446

    Article  Google Scholar 

  • Wilson ADM, Whattam EM, Bennet R, Visanuvimol L, Lauzon C, Bertram SM (2010) Behavioral correlations across activity, mating, exploration, aggression, and antipredator contexts in the European house cricket, Acheta domesticus. Behav Ecol Sociobiol 64:703–715

    Article  Google Scholar 

  • Winder VL, Pennington PL, Hurd MW, Wirth EF (2012) Fluoxetine effects on sheepshead minnow (Cyprinodon variegatus) locomotor activity. J Environ Health 47:51–58

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Brittney Logan for her assistance with data collection and fish care. They also thank Tori Doty, Nicole Greaney, Krystal Mannion, and Jodi Marks for their helpful feedback on an earlier version of this manuscript. Woon Yuen Koh provided statistical assistance. This work was funded by a University of New England Sponsored Programs grant to TLD (Grant # PDZ2).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Teresa L. Dzieweczynski.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dzieweczynski, T.L., Kane, J.L., Campbell, B.A. et al. Fluoxetine exposure impacts boldness in female Siamese fighting fish, Betta splendens . Ecotoxicology 25, 69–79 (2016). https://doi.org/10.1007/s10646-015-1568-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-015-1568-8

Keywords

  • Inadvertent pharmaceutical exposure
  • Fluoxetine
  • Behavioral consistency
  • Shy-bold continuum
  • Siamese fighting fish