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Signaling on Prozac: altered audience effects on male-male interactions after fluoxetine exposure in Siamese fighting fish

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Abstract

Selective serotonin reuptake inhibitors, such as fluoxetine, within the aquatic environment may adversely affect the health and behavior of exposed organisms. Most studies on the effects of inadvertent pharmaceutical exposure focus on the individual level rather than examining behavior within a network of individuals. Within communication networks, interactants send signals to multiple individuals, potentially altering, and being altered by, the behavior of nearby individuals. To address if fluoxetine interferes with communication within a network, male Siamese fighting fish interacted under three audience types (male, female, or no audience) and two exposure conditions (control, fluoxetine). In the control group, findings were similar to prior studies, with males altering gill flaring rate depending on the sex of the audience present. In the exposed group, gill flaring did not differ based on audience type and was lower overall compared to the control, suggesting a reduction in aggression. In contrast, both unexposed and exposed males performed more tail beats when a female audience was present, suggesting that fluoxetine has a context-specific effect on behavior. Behavioral changes during current interactions may affect behavior during later interactions as well as the outcome of future encounters with audience individuals. The influence of fluoxetine on total behavior within an interaction and loss of audience effect suggests it may generate broader changes in communication beyond the exposed individual, causing fitness consequences. This study stresses the importance of studying the effects of inadvertent pharmaceutical exposure on behavior in multiple social contexts to better understand its impacts on complex communication systems.

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References

  • Arnold KE, Boxall ABA, Brown AR, Cuthbert RJ, Gaw S, Hutchinson TH, Jobling S, Madden JC, Metcalfe CD, Naidoo V, Shore RF, Smits JE, Taggart MA, Thompson HM (2013) Assessing the exposure risk and impacts of pharmaceuticals in the environment on individuals and ecosystems. Biol Lett 9:20130492

  • Arnold KE, Brown AR, Ankley GT, Sumpter JP (2014) Medicating the environment: assessing risks of pharmaceuticals to wildlife and ecosystems. Philos Trans R Soc B 369:20130569

    Article  Google Scholar 

  • Barry MJ (2013) Effects of fluoxetine on the swimming and behavioral responses of the Arabian killifish. Ecotoxicology 22:425–532

    Article  CAS  PubMed  Google Scholar 

  • Bertucci F, Matos RJ, Dabelsteen T (2013) Knowing your audience affects male-male interactions in Siamese fighting fish (Betta splendens). Anim Cogn 17:229–236

    Article  PubMed  Google Scholar 

  • Bossus MC, Guler YZ, Short SJ, Morrison ER, Ford AT (2014) Behavioral and transcriptional changes in the amphipod Echinogammarus marinus exposed to two antidepressants, fluoxetine and sertraline. Aquat Toxicol 151:46–56

    Article  CAS  PubMed  Google Scholar 

  • Brodin T, Piovano S, Fick J, Klaminder J, Heynen M, Jonsson M (2014) Ecological effects of pharmaceuticals in aquatic systems—impacts through behavioral alterations. Philos Trans R Soc B 369:20130580

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Clotfelter ED, McNitt MM, Carpenter RE, Summers CH (2010) Modulation of monoamine neurotransmitters in fighting fish Betta splendens exposed to waterborne phytoestrogens. Fish Physiol Biochem 36:933–943

    Article  CAS  PubMed  Google Scholar 

  • Clotfelter ED, O’Hare EP, McNitt MH, Carpenter RE, Summers CH (2007) Serotonin decreases aggression via 5-HT1A receptors in the fighting fish, Betta splendens. Pharm Biochem Behav 87:222–231

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dabelsteen T (2005) Public, private or anonymous? Facilitating and countering eavesdropping. In: McGregor PK (ed) Animal communication networks. Cambridge University Press, Cambridge, pp 38–62

    Chapter  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  PubMed  Google Scholar 

  • Doutrelant C, McGregor PK, Oliveira RF (2001) The effect of an audience on intrasexual communication in male Siamese fighting fish, Betta splendens. Behav Ecol 12:283–286

    Article  Google Scholar 

  • Dubois F, Belzile A (2012) Audience effect alters male mating preferences in zebra finches (Taeniopygia guttata). PLoS ONE 7:e43697

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dzieweczynski TL, Earley RL, Green TM, Rowland WJ (2005) Audience effect is context dependent in Siamese fighting fish, Betta splendens. Behav Ecol 16:1025–1030

    Article  Google Scholar 

  • Dzieweczynski TL, Hebert OL (2012) Fluoxetine alters behavioral consistency of aggression and courtship in male Siamese fighting fish. Physiol Behav 107:92–97

    Article  CAS  PubMed  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 Contam Toxicol 64:316–326

    Article  CAS  PubMed  Google Scholar 

  • Dzieweczynski TL, Mannion KL, Greaney NE (2014) Audience effect on female-female interactions in Siamese fighting fish. Ethology 120:855–862

    Article  Google Scholar 

  • Dzieweczynski TL, Russell AM, Forrette LM, Mannion KL (2013) Male behavioural type affects female preference in Siamese fighting fish. Behav Ecol 25:136–141

    Article  Google Scholar 

  • Dzieweczynski TL, Walsh MM (2010) Audience type and receptivity affect male-female interactions in Siamese fighting fish. Ethology 116:10–18

    Article  Google Scholar 

  • Earley RL, Dugatkin LA (2002) Eavesdropping on visual cues in green swordtail (Xiphophorus helleri) fights: a case for networking. Proc R Soc Lond B 269:943–952

    Article  Google Scholar 

  • Elipot Y, Hinaux H, Callebert J, Rétaux S (2013) Evolutionary shift from fighting to foraging in blind cavefish through changes in the serotonin network. Curr Biol 23:1–10

    Article  CAS  PubMed  Google Scholar 

  • Gardner M, Comber S, Scrimshaw MD, Cartmell E, Lester J, Ellor B (2012) The significance of hazardous chemicals in wastewater treatment works effluents. Sci Total Environ 437:363–372

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Gunnarsson L, Jauhiainen A, Kristiansson E, Nerman O, Larsson DGJ (2008) Evolutionary conservation of human drug targets in organisms used for environmental risk assessments. Environ Sci Technol 42:5807–5813

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Johnson AC, Sumpter JP (2014) Putting pharmaceuticals into the wider context of challenges to fish populations in rivers. Philos Trans R Soc B 369:20130581

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  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

  • Kreke N, Dietrich DR (2008) Physiological endpoints for potential SSRI interactions in fish. Crit Rev Toxicol 38:215–247

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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 behaviour in Betta splendens. Adv Physiol Educ 31:353–363

    Article  Google Scholar 

  • Matessi G, Matos RJ, Peake TM, McGregor PK, Dabelsteen T (2010) Effects of social environment and personality on communication in male Siamese fighting fish in an artificial network. Anim Behav 79:43–49

    Article  Google Scholar 

  • Matos RJ, McGregor PK (2002) The effect of the sex of an audience on male-male displays of Siamese fighting fish (Betta splendens). Behaviour 139:1211–1221

    Article  Google Scholar 

  • Matos RJ, Schlupp I (2005) Performing in front of an audience: signalers and the social environment. In: McGregor PK (ed) Animal communication networks. Cambridge University Press, Cambridge, pp 63–83

    Chapter  Google Scholar 

  • McGregor PK, Peake TM (2000) Communication networks: social environments for receiving and signaling behavior. Acta Ethol 2:71–81

    Article  Google Scholar 

  • McGregor P (2005) Animal communication networks. Cambridge University Press, Cambridge

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Oliveira RF, McGregor PK, Latruffe C (1998) Know thine enemy: fighting fish gather information from observing conspecific interactions. Proc R Soc Lond B 265:1045–1049

    Article  Google Scholar 

  • Ophir A, Galef BG (2003) Female Japanese quail that “eavesdrop” on fighting males prefer losers to winners. Anim Behav 66:399–407

    Article  Google Scholar 

  • Plath M, Kromuszczynski K, Tiedemann R (2008) Audience effect alters male but not female mating preferences. Behav Ecol Sociobiol 63:381–399

    Article  Google Scholar 

  • Rand-Weaver M, Margiotta-Casaluci L, Patel A, Panter GH, Owen SF, Sumpter JP (2013) The read-across hypothesis and environmental risk assessment of pharmaceuticals. Environ Sci Technol 47:12297–12304

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Shenoy K, Crowley PH (2011) Endocrine disruption of male mating signals: ecological and evolutionary implications. Funct Biol 25:433–448

    Article  Google Scholar 

  • Simpson MJA (1968) The display of the Siamese fighting fish, Betta splendens. Anim Behav Monogr 1:1–73

    Article  Google Scholar 

  • Snekser JL, McRobert SP, Clotfelter ED (2006) Social partner preferences of male and female fighting fish (Betta splendens). Behav Process 72:38–41

    Article  CAS  Google Scholar 

  • Stevenson LM, Brown AC, Montgomery TM, Clotfelter ED (2011) Reproductive consequences of exposure to waterborne phytoestrogens in male fighting fish, Betta splendens. Arch Environ Contam Toxicol 60:501–510

    Article  CAS  PubMed  Google Scholar 

  • Summers CH, Korzan WJ, Watt MJ, Forster GL, Øverli Ø, Höglund E, Larson ET, Ronan PJ, Matter JM, Summers TR, Renner KJ, Greenberg N (2005) Does serotonin influence aggression? Comparing regional activity before and during social interaction. Physiol Biochem Zool 78:679–694

  • Sumpter JP, Donnachi RL, Johnson AC (2014) The appartently very variable potency of the anti-depressant fluoxetine. Aquat Toxicol 151:57–60

    Article  CAS  PubMed  Google Scholar 

  • Townsend SW, Zuberbühler K (2009) Audience effects in chimpanzee copulation calls. Commun Integr Biol 2:282–284

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang Y, Takai R, Yoshioka H, Shirabe K (2006) Characterization and expression of serotonin transporter genes in zebrafish. Tohoku J Exp Med 208:267–274

    Article  CAS  PubMed  Google Scholar 

  • Weinberger J III, Klaper R (2014) Environmental concentrations of the selective serotonin reuptake inhibitor fluoxetine impact specific behaviours involved in reproduction, feeding and predator avoidance in the fish Pimephales promelas (fathead minnow). Aquat Toxicol 151:77–83

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zaccaroni M, Binazzi R, Massolo A, Dessi-Fulgheri F (2013) Audience effect on aerial alarm calls in the monogamous red-legged partridge. Ethol Ecol Evol 25:366–376

    Article  Google Scholar 

  • Zuberbühler K (2008) Audience effects. Curr Biol 18:R189–R190

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors thank Amy Keirstead for analyzing water samples to determine EE2 concentration. Brennah Campbell, Sydney Farrin, Jessica Kane, Haley Lamonica, and two anonymous reviewers provided helpful feedback on an earlier version of this manuscript. This work was funded by a UNE OSP grant to TLD.

Compliance with ethical standards

This experiment was approved by the University of New England’s IACUC committee and is covered by protocol UNE-20130910DZIET.

Ethical approval

All procedures performed in this study were in accordance with the ethical standards of the University of New England where this work was conducted and covered under protocol UNE-20130910DZIET.

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Authors and Affiliations

  1. Department of Marine Sciences, University of New England, 11 Hills Beach Rd, Biddeford, ME, 04005, USA

    Nicole E. Greaney & Krystal L. Mannion

  2. Department of Psychology, University of New England, 11 Hills Beach Rd, Biddeford, ME, 04005, USA

    Krystal L. Mannion & Teresa L. Dzieweczynski

Authors
  1. Nicole E. Greaney
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  2. Krystal L. Mannion
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  3. Teresa L. Dzieweczynski
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Correspondence to Teresa L. Dzieweczynski.

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Communicated by A. Pilastro

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Greaney, N.E., Mannion, K.L. & Dzieweczynski, T.L. Signaling on Prozac: altered audience effects on male-male interactions after fluoxetine exposure in Siamese fighting fish. Behav Ecol Sociobiol 69, 1925–1932 (2015). https://doi.org/10.1007/s00265-015-2005-y

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  • DOI: https://doi.org/10.1007/s00265-015-2005-y

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