Skip to main content
SpringerLink
Log in

Mating under the influence: male Siamese fighting fish prefer EE2-exposed females

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Countless pharmaceuticals and endocrine disrupting chemicals (EDCs) exist on the market with more added each day. Many of these compounds are not removed during the wastewater treatment process and enter bodies of water in their active form. EDCs are known to have physiological and behavioral effects in exposed organisms. Exposure to the synthetic estrogen 17α-ethinylestradiol (EE2), a common EDC found in birth control pills, has been found to lead to population collapse after only a few generations in some fish species. Mechanisms identified as potential driving forces for collapse include feminization of males and altered fecundity in both sexes. However, an additional way in which EE2 could lead to population collapse is by altering courtship behavior, which could then change mating preferences and decrease mating opportunities. The current study had the following objectives: determine if exposing female Siamese fighting fish, Betta splendens, to EE2 changes mate choice in males; assess if the dose and duration of female exposure matters; and examine if exposing males to EE2 influences their mating preferences. Both unexposed and exposed males were presented with pairs of females that differed in EE2 dose and exposure duration. The results indicate that males were more responsive to EE2-exposed females than unexposed females, with males being most responsive to females exposed to the low versus high dose. Furthermore, exposed males responded less overall than unexposed males. If EE2 concentration increases in the environment, the likelihood of successful mating could decrease and, therefore, potentially lead to adverse population impacts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

All data analyzed during this study are available via the Open Science Framework (osf.io/e3qj9).

References

  • Adeel M, Song X, Wang X, Francis D, Yang Y (2017) Environmental impact of estrogens on human, animal and plant life: a critical review. Environ Intern 99:107–119

    Article  CAS  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, NJ

    Google Scholar 

  • 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 

  • Asarian L, Geary N (2002) Cyclic estradiol treatment normalizes body weight and restores physiological patterns of spontaneous feeding and sexual receptivity in ovariectomized rats. Horm Behav 42:461–471

    Article  CAS  Google Scholar 

  • Baronti C, Curini R, D’Ascenzo G, Di Corcia A, Gentili A, Samperi R (2000) Monitoring natural and synthetic estrogens at activated sludge sewage treatment plants and in a receiving river water. Environ Sci Technol 34:5059–5066

    Article  CAS  Google Scholar 

  • Bell AM (2001) Effects of an endocrine disrupter on courtship and aggressive behavior of male three-spined stickleback, Gasterosteus aculeatus. Anim Behav 62:775–780

    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 

  • Brian JV, Augley JJ, Braithwaite VA (2006) Endocrine disrupting effects on the nesting behavior of male three-spined stickleback Gasterosteus aculeatus. J Fish Biol 68:1883–1890

    Article  CAS  Google Scholar 

  • Ciocan CM, Cubero-Leon E, Puinean AM, Hill EM, Minier C, Osada M et al. (2010) Effects of estrogen exposure in mussels, Mytilus edulis, at different stages of gametogenesis. Environ Pollut 158:2977–84

    Article  CAS  Google Scholar 

  • Clotfelter ED, Curren LJ, Murphy CE (2006) Mate choice and spawning success in the fighting fish Betta splendens: the importance of body size, display behavior and nest size. Ethology 112:1170–1178

    Article  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  Google Scholar 

  • Coe TS, Hamilton PB, Hodgson D, Paull GC, Stevens JR, Sumner K, Tyler CR (2008) An environmental estrogen alters reproductive hierarchies, disrupting sexual selection in group-spawning fish. Environ Sci Technol 42:5050–5025

    Article  CAS  Google Scholar 

  • Colman JR, Baldwin D, Johnson LL, Scholz NL (2009) Effects of the synthetic estrogen, 17ɑ-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). Aquat Toxicol 91:346–354

    Article  CAS  Google Scholar 

  • Doutrelant C, McGregor PK (2000) Eavesdropping and mate choice in female fighting fish. Behaviour 137:1655–1669

    Article  Google Scholar 

  • Doyle TJ, Bowman JL, Windell VL, McLean DJ, Kim KH (2013) Transgenerational effects of di-(2-ethylhexyl)phthalate on testicular germ cell associations and spermatogonial stem cells in mice. Biol Reprod 88:112

    Article  Google Scholar 

  • Dzieweczynski TL, Gill CE, Walsh MM (2010) The nest matters: the influence of reproductive status on decision-making to conflicting stimuli in male Siamese fighting fish. Behaviour 147:805–823

    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 Contam Toxicol 64:316–326

    Article  CAS  Google Scholar 

  • Dzieweczynski TL, Hentz KB, Logan B, Hebert OL (2014) Chronic exposure to 17α-ethinylestradiol reduces behavioral consistency in male Siamese fighting fish. Behaviour 151:633–651

    Article  Google Scholar 

  • Dzieweczynski TL, Kane JL (2017) The bachelorette: female Siamese fighting fish avoid males exposed to an estrogen mimic. Behav Proc 140:169–173

    Article  Google Scholar 

  • Dzieweczynski TL, LaMonica HJ (2016) Court like you mean it: male Siamese fighting fish are less attentive to courting males that have been exposed to an estrogen mimic. Ethology 122:991–998

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Edward DA, Chapman T (2011) The evolution and significance of male mate choice. Trends Ecol Evol 26:647–654

    Article  Google Scholar 

  • Frye CA, Bo E, Calamandrei G et al. (2012) Endocrine disruptors: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J Neuroendocrinol 24:144–159

    Article  CAS  Google Scholar 

  • Gaw S, Thomas KV, Hutchinson TH (2014) Sources, impacts and trends in pharmaceuticals in the marine and coastal environment. Philos Trans R Soc B 369:20130572

    Article  Google Scholar 

  • Gleason TR, Nacci NE (2001) Risks of endocrine-disrupting compounds to wildlife: extrapolating from effects on individuals to population response. Hum Ecol Risk Assess 7:1027–1042

    Article  CAS  Google Scholar 

  • Guillette LJ, Gross TS, Gross DA, Rooney AA, Percival HF (1995) Gonadal steroidogenesis in vitro from juvenile alligators obtained from contaminated or control lakes. Environ Health Pers 103:3136

    Google Scholar 

  • Hunt J, Breuker CJ, Sadowski JA, Moore AJ (2009) Male-male competition, female mate choice and their interaction: determining total sexual selection. J Evol Biol 22:14

    Article  Google Scholar 

  • Jaroensutasinee M, Jaroensutasinee K (2001) Sexual size dimorphism and male contest in wild Siamese fighting fish. J Fish Biol 59:1614–1621

    Article  Google Scholar 

  • Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP (1998) Widespread sexual disruption in wild fish. Environ Sci Technol 32:2498–2506

    Article  CAS  Google Scholar 

  • Kidd KA, Blanchfield PJ, Mills KH, Palace VP, Evans RE, Lazorchak JM, Flick RW (2007) Collapse of a fish population after exposure to a synthetic estrogen. Proc Natl Acad Sci USA 104:8897–8901

    Article  CAS  Google Scholar 

  • Kime DE (1998) Endocrine disruption in fish. Kluwer, Boston

    Book  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 

  • Kristensen T, Baatrup E, Bayley M (2005) 17α-ethinylestradiol reduces the competitive reproductive fitness of the male guppy (Poecilia reticulata). Biol Reprod 72:150–156

    Article  CAS  Google Scholar 

  • La Farre M, Perez S, Kantiani L, Barcelo D (2008) Fate and toxicity of emerging pollutants, their metabolites and transformation products in the aquatic environment. Trends Anal Chem 27:991–1007

    Article  CAS  Google Scholar 

  • Lai KM, Scrimshaw MD, Lester JN (2002) Prediction of the bioaccumulation factors and body burden of natural and synthetic estrogens in aquatic organisms in the river systems. Sci Total Environ 289:159–168

    Article  CAS  Google Scholar 

  • Länge R, Hutchinson TH, Croudace CP, Siegmund F, Schweinfurth H, Hampe P, Panther GH, Sumpter JP (2001) Effects of the synthetic estrogen 17α-ethinylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ Toxicol Chem 20:1216–1227

    Article  Google Scholar 

  • Larsson DGJ, Adolfsson-Erici M, Parkkonen J, Pettersson M, Berg AH, Olsson P-E, Förlin L (1999) Ethinylestradiol: an undesired fish contraceptive? Aquat Toxicol 45:91–97

    Article  CAS  Google Scholar 

  • Lehtonen TK, Svensson PA, Wong BBM (2011) Both male and female identity influence variation in male signaling effort. BMC Evol Biol 11:233

    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

  • Mills LJ, Chichester C (2005) Review of evidence: are endocrine disrupting chemicals in the aquatic environment impacting fish populations? Sci Total Environ 343:1–34

    Article  CAS  Google Scholar 

  • Muller M, Rabenoelina F, Balaguer P, Patureau D, Lemenach K, Budzinski H, Barcelo D, De Alda ML, Kuster M, Delgenes JP, Hernandez-Raquet G (2008) Chemical and biological analysis of endocrine-disrupting hormones and estrogenic activity in an advanced sewage treatment plant. Environ Toxicol Chem 27:1649–1658

    Article  CAS  Google Scholar 

  • Nash JP, Kime DE, van der Ven LT, Wester PW, Brion F, Maack G, Stahlschmidt-Allner P, Tyler CR (2004) Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ Health Perspect 112:1725–1733

    Article  CAS  Google Scholar 

  • Palace VP, Evans RE, Wautier KG, Mills KH, Blanchfield PJ, Park BJ et al. (2009) Interspecies differences in biochemical, histopathological, and population responses in four wild fish species exposed to ethinylestradiol added to a whole lake. Can J Fish Aquat Sci 66:1920–1935

    Article  CAS  Google Scholar 

  • Persaud KN, Galef Jr. BG (2005) Female Japanese quail (Coturnix japonica) mated with males that harassed them are unlikely to lay fertilized eggs. J Comp Psychol 119:440–446

    Article  Google Scholar 

  • Peterson EK, Buckwalter DB, Kerby JL, LeFauve MK, Varian-Ramos CW, Swaddle JP (2017) Integrative behavioral ecotoxicology: bringing together fields to establish new insight to behavioral ecology, toxicology, and conservation. Curr Zool. https://doi.org/10.1093/cz/zox010

  • Purdom CE, Hardiman PA, Bye VJ, Eno NC, Tyler CR, Sumpter JP (1994) Estrogenic effects of effluents from sewage treatment works. Chem Ecol 8:275–285

    Article  CAS  Google Scholar 

  • Rowland WJ (1982) Mate choice by male sticklebacks, Gasterosteus aculeatus. Anim Behav 30:1093–1098

    Article  Google Scholar 

  • Saaristo M, Craft JA, Lehtonen KK, Lindstrom K (2010) Exposure to 17α-ethinyl oestradiol impairs courtship and aggressive behaviour of male sand gobies (Pomatoschistus minutus). Chemosphere 79:541–546

    Article  CAS  Google Scholar 

  • Saaristo M, Craft JM, Lehtonen KK, Lindström K (2009) Sand goby (Pomatoschistus minutus) males exposed to an endocrine disrupting chemical fail in nest and mate competition. Horm Behav 56:315–321

    Article  CAS  Google Scholar 

  • Salierno JD, Kane AS (2009) 17α-ethinyloestradiol alters reproductive behaviours, circulating hormones, and sexual morphology in male fathead minnows (Pimephales promelas). Environ Toxicol Chem 28:953–961

    Article  CAS  Google Scholar 

  • Shore LS, Gurevitz M, Shemesh M (1993) Estrogen as an environmental pollutant. Bull Environ Contam Toxicol 51:361–366

    Article  CAS  Google Scholar 

  • Silva P, Rocha MJ, Cruzeiro C, Malhão F, Reis B, Urbatzka R, Monteiro RAF, Rocha E (2012) Testing the effects of ethinylestradiol and of an environmentally relevant mixture of xenoestrogens as found in the Douro River (Portugal) on the maturation of fish gonads—a stereological study using the zebrafish (Danio rerio) as model. Aquat Toxicol 124:1–10

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Söffker M, Stevens JR, Tyler CR (2012) Comparative breeding and behavioral responses to ethinylestradiol exposure in wild and laboratory maintained zebrafish (Danio rerio) populations. Environ Sci Technol 46:11377–11383

    Article  CAS  Google Scholar 

  • Stapley J (2008) Female mountain log skinks are more likely to mate with males that court more, not males that are dominant. Anim Behav 75:529–538

    Article  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  Google Scholar 

  • Sumpter JP (2005) Endocrine disruptors in the aquatic environment: an overview. Acta Hydroch Hydrob 33:9–16

    Article  CAS  Google Scholar 

  • Ternes TA, Kreckel P, Mueller J (1999) Behavior and occurrence of estrogens in municipal sewage treatment plants--II. Aerobic batch experiments with activated sludge. Sci Total Environ 12:91–99

    Article  Google Scholar 

  • Tyler CR, Jobling S, Sumpter JP (1998) Endocrine disruption in wildlife: a critical review of the evidence. Crit Rev Toxicol 28:319–361

    Article  CAS  Google Scholar 

  • Verbeek P, Iwamoto T, Murakami N (2008) Differences in aggression between wild-type and domesticated fighting fish are context dependent. Anim Behav 73:75–83

    Article  Google Scholar 

  • Volkova K, Reyhanian N, Kot-Wasik A, Olsén H, Porsch-Hällström I, Hallgren S (2012) Brain circuit imprints of developmental 17α-ethinylestradiol exposure in guppies (Poecilia reticulata): persistent effects on anxiety but not on reproductive behavior. Gen Comp Endocrinol 178:282–290

    Article  CAS  Google Scholar 

  • Zala SM, Penn DJ (2004) Abnormal behaviors induced by chemical pollution: a review of the evidence and new challenges. Anim Behav 68:649–664

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Haley LaMonica for her assistance in running behavioral trials. They also thank Jessica Kane, Kelley Portrais, Megan Stevens, and two anonymous reviewers for their feedback on a previous version of this manuscript. Amy Keirstead and Molly Wright were instrumental in creating the EE2 solution and analyzing EE2 in water samples.

Author information

Authors and Affiliations

  1. Department of psychology, University of New England, 11 Hills Beach Road, Biddeford, ME, 04005, USA

    Rebecca A. Cram, Jaslynn M. Lawrence & Teresa L. Dzieweczynski

Authors
  1. Rebecca A. Cram
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jaslynn M. Lawrence
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Teresa L. Dzieweczynski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Teresa L. Dzieweczynski.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Animal care and experimental protocols were approved by the UNE IACUC and covered under protocol UNE-20130910DZIET.

Informed consent

All authors have approved this version of the work.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cram, R.A., Lawrence, J.M. & Dzieweczynski, T.L. Mating under the influence: male Siamese fighting fish prefer EE2-exposed females. Ecotoxicology 28, 201–211 (2019). https://doi.org/10.1007/s10646-018-02012-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-018-02012-y

Keywords

Search

Navigation