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Effects of fluoxetine on the swimming and behavioural responses of the Arabian killifish

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Abstract

The selective serotonin reuptake inhibitor fluoxetine has frequently been detected in surface waters around the world. Fluoxetine modulates levels of serotonin, a neurotransmitter that regulates several important physiological and behavioural processes including fear and anxiety, aggression, locomotion and feeding. In this study, groups of sub-adult Arabian killifish (Aphanius dispar) were exposed to either 0, 0.03, 0.3 or 3 μg/L fluoxetine hydrochloride for 7 days and their swimming behaviour and social interactions videotaped in a circular arena. The fish were subsequently exposed to a predator alarm chemical (from dragonfly larvae fed with A. dispar) and their short-term responses recorded. The video was analysed using the open-sourced software program Ctrax which objectively quantified swimming and social behaviours. Aggression (chasing behaviour was significantly reduced at 3.0 μg/L fluoxetine. After the addition of the predator alarm chemicals fish responded quickly, increasing the percentage of time spent drifting or motionless and reducing average swimming velocity. Controls and fish exposed to 0.03 or 3 μg/L fluoxetine reduced swimming speed by 20–30 % but returned to pre-exposure velocities within 6 min. Fish exposed to 0.3 μg/L fluoxetine reduced swimming speed by 38 % after addition of the predator alarm and did not return to pre-exposure speeds during the recording period (19 min). Schooling behaviour was also affected by fluoxetine and predator alarm with fish exposed to 0.3 μg/L fluoxetine significantly reducing nearest neighbour distance and swimming speed relative to nearest neighbour the following addition of the predator alarm.

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References

  • Azmitia EC (1999) Serotonin neurons, neuroplasticity, and homeostasis of neural tissue. Neuropsychopharmacology 21:33S–45S

    CAS  Google Scholar 

  • Barbosa A Jr, Alves FL, de Pereira SF A, Ide LM, Hoffmann A (2012) Behavioral characterization of the alarm reaction and anxiolytic-like effect of acute treatment with fluoxetine in piauçu fish. Physiol Behav 105:784–790

    Article  CAS  Google Scholar 

  • Barry MJ (2011) Effects of copper, zinc and dragonfly kairomone on growth rate and induced morphology of Bufo arabicus tadpoles. Ecotoxicol Environ Saf 74:918–923

    Article  CAS  Google Scholar 

  • Branson K, Robie AA, Bender J, Perona P, Dickinson MH (2009) High-throughput ethomics in large groups of Drosophila. Nat Methods 6:451–457

    Article  CAS  Google Scholar 

  • Brooks BW, Foran CM, Richards SM, Weston J, Turner PK, Stanley JK, Solomon KR, Slattery M, La Point TW (2003) Aquatic ecotoxicology of fluoxetine. Toxicol Lett 142:169–183

    Article  CAS  Google Scholar 

  • Brown GE, Godin J-GJ (1997) Anti-predator responses to conspecific and heterospecific skin extracts by threespine sticklebacks: alarm pheromones revisited. Behaviour 134:1123–1134

    Article  Google Scholar 

  • Brown GE, Paige JA, Godin J-GJ (2000) Chemically mediated predator inspection behaviour in the absence of predator visual cues by a characin fish. Anim Behav 60:315–321

    Article  Google Scholar 

  • Brown GE, Rive AC, Ferrari MCO, Chivers DP (2006) The dynamic nature of antipredator behavior: prey fish integrate threat-sensitive antipredator responses within background levels of predation risk. Behav Ecol Sociobiol 61:9–16

    Article  Google Scholar 

  • Calabrese EJ (2005) Paradigm lost, paradigm found: the re-emergence of hormesis as a fundamental dose response model in the toxicological sciences. Environ Pollut 138:378–411

    Article  CAS  Google Scholar 

  • Chivers DP, Wisenden BD, Smith RJF (1995) The role of experience in the response of fathead minnows (Pimephales promelas) to skin extract of Iowa darters (Etheostoma exile). Behaviour 132:665–674

    Article  Google Scholar 

  • Daughton CG, Ternes TA (1999) Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ Health Perspect 107:907–938

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Delville Y, Melloni RH, Ferris CF (1998) Behavioral and neurobiological consequences of social subjugation during puberty in golden hamsters. J Neurosci 18:2667–2672

    CAS  Google Scholar 

  • Dulawa SC, Holick KA, Gundersen B, Hen R (2004) Effects of chronic fluoxetine in animal models of anxiety and depression. Neuropsychopharmacology 29:1321–1330

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fernandes D, Schnell S, Porte C (2011) Can pharmaceuticals interfere with the synthesis of active androgens in male fish? an in vitro study. Mar Pollut Bull 62:2250–2253

    Article  CAS  Google Scholar 

  • Ferris CF (1996) Serotonin diminishes aggression by suppressing the activity of the vasopressin system. Ann N Y Acad Sci 794:98–103

    Article  CAS  Google Scholar 

  • Ferris CF, Axelson JF, Martin AM, Roberge LF (1989) Vasopressin immunoreactivity in the anterior hypothalamus is altered during the establishment of dominant/subordinate relationships between hamsters. Neuroscience 29:675–683

    Article  CAS  Google Scholar 

  • Filby A, Paull G, Hickmore T, Tyler C (2010) Unravelling the neurophysiological basis of aggression in a fish model. BMC Genomics 11:498

    Article  Google Scholar 

  • Francis RC (1988) On the relationship between aggression and social dominance. Ethology 78:223–237

    Article  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 

  • Gilmour KM, DiBattista JD, Thomas JB (2005) Physiological causes and consequences of social status in salmonid fish. Integr Comp Biol 45:263–273

    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 

  • Henry TB, Black MC (2007) Acute and chronic toxicity of fluoxetine (selective serotonin reuptake inhibitor) in western mosquitofish. Arch Environ Contam Toxicol 54:325–330

    Article  Google Scholar 

  • Herbert-Read JE, Perna A, Mann RP, Schaerf TM, Sumpter DJT, Ward AJW (2011) Inferring the rules of interaction of shoaling fish. Proc Nat Acad Sci 108:18726–18731

    Article  CAS  Google Scholar 

  • Johnson DM (1991) Behavioral ecology of larval dragonflies and damselflies. Trends Ecol Evol 6:8–13

    Article  CAS  Google Scholar 

  • Jones TC, Akoury TS, Hauser CK, Neblett MF II, Linville BJ, Edge AA, Weber NO (2011) Octopamine and serotonin have opposite effects on antipredator behavior in the orb-weaving spider, Larinioides cornutus. J Comp Physiol 197:819–825

    Article  CAS  Google Scholar 

  • Kania BF, Gralak MA, Wielgosz M (2012) Four-week fluoxetine (SSRI) exposure diminishes aggressive behaviour of male siamese fighting fish (Betta splendens). Behav Brain Sci 2:185–190

    Article  CAS  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 Technol 36:1202–1211

    Article  CAS  Google Scholar 

  • Kwon JW, Armbrust KL (2006) Laboratory persistence and fate of fluoxetine in aquatic environments. Environ Toxicol Chem 25:2561–2568

    Article  CAS  Google Scholar 

  • Leonardo ED, Hen R (2006) Genetics of affective and anxiety disorders. Ann Rev Psychol 57:117–137

    Article  CAS  Google Scholar 

  • Lillesaar C (2011) The serotonergic system in fish. J Chem Neuroanat 41:294–308

    Article  CAS  Google Scholar 

  • Little EE, Finger SE (1990) Swimming behavior as an indicator of sublethal toxicity in fish. Environ Toxicol Chem 9:13–19

    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 Edu 31:358–363

    Article  Google Scholar 

  • Magellan K, Kaiser H (2010) Male aggression and mating opportunity in a poeciliid fish. Afr Zool 45:18–23

    Article  Google Scholar 

  • Maximino C, de Brito TM, Colmanetti R, Pontes AAA, de Castro HM, de Lacerda RIT, Morato S, Gouveia A Jr (2010) Parametric analyses of anxiety in zebrafish scototaxis. Behav Brain Res 210:1–7

    Article  Google Scholar 

  • Mennigen JA, Stroud P, Zamora JM, Moon TW, Trudeau VL (2011) Pharmaceuticals as neuroendocrine disruptors: lessons learned from fish on prozac. J Toxicol Environ Health 14:387–412

    Article  CAS  Google Scholar 

  • Painter MM, Buerkley MA, Julius ML, Vajda AM, Norris DO, Barber LB, Furlong ET, Schultz MM, Schoenfuss HL (2009) Antidepressants at environmentally relevant concentrations affect predator avoidance behavior of larval fathead minnows (Pimephales promelas). Environ Toxicol Chem 28:2677–2684

    Article  CAS  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 

  • Pitcher TJ (1992) Behaviour of teleost fishes. Springer, London

    Google Scholar 

  • Relyea RA (2004) Synergistic impacts of malathion and predatory stress on six species of north American tadpoles. Environ Toxicol Chem 23:1080–1084

    Article  CAS  Google Scholar 

  • Richendrfer H, Pelkowski SD, Colwill RM, Creton R (2012) On the edge: pharmacological evidence for anxiety-related behavior in zebrafish larvae. Behav Brain Res 228:99–106

    Article  CAS  Google Scholar 

  • Rosemberg DB, Rico EP, Mussulini BHM, Piato ÂL, Calcagnotto ME, Bonan CD, Dias RD, Blaser RE, Souza DO, de Oliveira DL (2011) Differences in spatio-temporal behavior of zebrafish in the open tank paradigm after a short-period confinement into dark and bright environments. PLoS ONE 6:e19397

    Article  CAS  Google Scholar 

  • Sackerman J, Donegan JJ, Cunningham CS, Nguyen NN, Lawless K, Long A, Benno RH, Gould GG (2010) Zebrafish behavior in novel environments: effects of acute exposure to anxiolytic compounds and choice of Danio rerio line. Int J Comp Psychol 23:43–61

    Google Scholar 

  • Scott GR, Sloman KA, Rouleau C, Wood CM (2003) Cadmium disrupts behavioural and physiological responses to alarm substance in juvenile rainbow trout (Oncorhynchus mykiss). J Exp Biol 206:1779–1790

    Article  CAS  Google Scholar 

  • Semsar K, Perreault HAN, Godwin J (2004) Fluoxetine-treated male wrasses exhibit low AVT expression. Brain Res 1029:141–147

    Google Scholar 

  • Smith RJF (1992) Alarm signals in fishes. Rev Fish Biol Fish 2:33–63

    Article  Google Scholar 

  • Spence R, Gerlach G, Lawrence C, Smith C (2008) The behaviour and ecology of the zebrafish, Danio rerio. Biol Rev Camb Philos Soc 83:13–34

    Google Scholar 

  • Stanley JK, Ramirez AJ, Chambliss CK, Brooks BW (2007) Enantiospecific sublethal effects of the antidepressant fluoxetine to a model aquatic vertebrate and invertebrate. Chemosphere 69:9–16

    Article  CAS  Google Scholar 

  • Templeton CN, Shriner WM (2004) Multiple selection pressures influence Trinidadian guppy (Poecilia reticulata) antipredator behavior. Behav Ecol 15:673–678

    Article  Google Scholar 

  • Teplitsky C, Piha H, Laurila A, Merilä J (2005) Common pesticide increases costs of antipredator defenses in Rana temporaria tadpoles. Environ Sci Technol 39:6079–6085

    Article  CAS  Google Scholar 

  • Warner RE (1966) Behavioural pathology in fish: a quantitative study of sublethal pesticide toxication. Blackwell, Oxford

    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

    CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by an internal Grant from Sultan Qaboos University (IG/SCI/BIOL/12/03).

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The author declares that he has no conflict of interest.

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Correspondence to Michael J. Barry.

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Barry, M.J. Effects of fluoxetine on the swimming and behavioural responses of the Arabian killifish. Ecotoxicology 22, 425–432 (2013). https://doi.org/10.1007/s10646-012-1036-7

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