Chronic exposure to 17α-ethinylestradiol reduces behavioral consistency in male Siamese fighting fish
In: BehaviourSearch for other papers by Teresa L. Dzieweczynski in
Current site
Google Scholar
Search for other papers by Kimberly B. Hentz in
Current site
Google Scholar
Search for other papers by Brittney Logan in
Current site
Google Scholar
Search for other papers by Olivia L. Hebert in
Current site
Google Scholar
Both acute and chronic exposure to 17α-ethinylestradiol (EE2), one of the primary active ingredients of birth control pills, decreases courtship and aggression in males of aquatic species. However, how exposure affects behavioral consistency over time is not commonly addressed. To examine the effects of chronic EE2 exposure on behavioral consistency, adult male Siamese fighting fish, Betta splendens, received multiple trials with a dummy male and dummy female presented simultaneously both before and after chronic exposure to a nominal dose (10 ng/l) of EE2. The responses of exposed males were compared before and after exposure and against those of a group of unexposed, control males. Male-directed and female-directed behaviors were reduced after 28 days of EE2 exposure. More importantly, chronic EE2 exposure had dramatic effects on consistent individual differences in female-directed and male-directed behaviors. Repeatability values were markedly lower and level of response was less correlated in the EE2 group, suggesting that exposure disrupts both between-individual variation and behavioral consistency. These results cannot be explained by a temporal effect as they were not found in the control group of unexposed males. This study demonstrates that EE2 exposure may have effects beyond a reduction in overall response. It also demonstrates the importance of studying the effects of chemical exposure on multiple time scales as acute exposure to EE2 affects the consistency of only female-directed behaviors in this species whereas chronic exposure affects consistency of both female-directed and male-directed behavior. Finally, this study suggests that males in this species may differ in their sensitivity, an important area for future research.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
-
Becker W.A. (1984). Manual of quantitative genetics, 4th edn. â Academic Enterprises, Pullman, WA.
-
Bell A.M. (2001). Effects of an endocrine disrupter on courtship and aggressive behaviour of male three-spined stickleback, Gasterosteus aculeatus. â Anim. Behav. 62: 775-780.
-
Bell A.M. (2004). An endocrine disrupter increases growth and risky behavior in three-spined stickleback (Gasterosteus aculeatus). â Horm. Behav. 45: 108-114.
-
Bell A.M., Sih A. (2007). Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). â Ecol. Lett. 10: 828-834.
-
Bergmüller R., Taborsky M. (2010). Animal personalities due to social niche specialization. â Trends Ecol. Evol. 25: 504-511.
-
Biro P.A., Adriaenssens B. (2013). Predictability as a personality trait: consistent differences in intraindividual behavioral variation. â Am. Nat. 182: 621-629.
-
Boake C.R.B. (1989). Repeatability: its role in evolutionary studies of mating behavior. â Evol. Ecol. 3: 173-182.
-
Bolnick D.I., Amarasekare P., Araujo M.S., Burger R., Levine J., Novak M. et al., (2011). Why intraspecific trait variation matters in community ecology. â Trends Ecol. Evol. 26: 183-192.
-
Breckels R.D., Neff B.D. (2010). Pollution-induced behavioral effects in the brown bullhead (Ameiurus nebulosus). â Ecotoxicology 19: 1337-1346.
-
Brian J.V., Augley J.J., Braithwaite V.A. (2006). Endocrine disrupting effects on the nesting behaviour of male three-spined stickleback Gasterosteus aculeatus. â J. Fish. Biol. 68: 1883-1890.
-
Clotfelter E.D., Bell A.M., Levering K.R. (2004). The role of animal behaviour in the study of endocrine-disrupting chemicals. â Anim. Behav. 68: 665-676.
-
Clotfelter E.D., McNitt M.M., Carpenter R.E., Summers C.H. (2010). Modulation of monoamine neurotransmitters in fighting fish Betta splendens exposed to waterborne phytoestrogens. â Fish Physiol. Biochem. 36: 933-943.
-
Clotfelter E.D., Rodriguez A.C. (2006). Behavioral changes in fish exposed to phytoestrogens. â Environ. Poll. 144: 833-839.
-
Coe T.S., Hamilton P.B., Hodgson D., Paull G.C., Stevens J.R., Sumner K., Tyler C.R. (2008). An environmental oestrogen alters reproductive hierarchies, disrupting sexual selection in a group-spawning fish. â Environ. Sci. Technol. 42: 5020-5025.
-
Colman J.R., Baldwin D., Johnson L.L., Scholz N.L. (2009). Effects of the synthetic estrogen, 17α-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). â Aquat. Toxicol. 91: 346-354.
-
Coppens C.M., deBoer S.F., Koolhaas J.M. (2010). Coping styles and behavioral flexibility: towards underlying mechanisms. â Phil. Trans. Roy. Soc. Lond. B 365: 4021-4028.
-
Cote J., Clobert J., Brodin T., Fogarty S., Sih A. (2010). Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. â Phil. Trans. Roy. Soc. Lond. B 365: 4065-4076.
-
Daughton C.G., Brooks B.W. (2011). Active pharmaceutical ingredients and aquatic organisms. â In: Environmental contaminants in biota: interpreting tissue concentrations, 2nd edn ( Beyer W.N., Meador J.P., eds). Taylor & Francis, Boca Raton, FL, p. 286-347.
-
Denny J.S., Tapper M.A., Schmieder P.K., Hornung M.W., Jensen K.M., Ankley G.T., Henry T.R. (2005). Comparison of relative binding affinities of endocrine active compounds to fathead minnow and rainbow trout estrogen receptors. â Environ. Toxicol. Chem. 24: 2948-2953.
-
Dingemanse N.J., Wolf M. (2013). Between-individual differences in behavioral plasticity within populations: causes and consequences. â Anim. Behav. 85: 1031-1039.
-
Duckworth R.A. (2009). The role of behavior in evolution: a search for mechanism. â Evol. Ecol. 23: 513-531.
-
Dzieweczynski T.L., Gill C.E., Walsh M.M. (2010). The nest matters: the influence of reproductive status on decision-making to conflicting stimuli in male Siamese fighting fish. â Behaviour 147: 805-823.
-
Dzieweczynski T.L., Hebert O.L. (2013). The effects of short-term exposure to an endocrine disrupter on behavioral consistency in juvenile and adult male Siamese fighting fish. â Arch. Environ. Toxicol. Chem. 64: 316-326.
-
Dzieweczynski T.L., Leopard A.M. (2010). The effectiveness of dummy vs. live conspecifics on consistent individual differences in decision making to conflicting stimuli in male Siamese fighting fish. â Behav. Proc. 85: 83-89.
-
Falconer D.S., Mackay T.F.C. (1996). Introduction to quantitative genetics, 4th edn. â Pearson Prentice Hall, Harlow.
-
Frye C.A., Bo E., Calamandrei G., Calzà L., Dessi-Fulgheri F., Fernández M., Fusani L., Kah O., Kajta M., Le Page Y., Patisau H.B., Venerosi A., Wojtowicz A.K., Panzica G.C. (2011). Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behavior and neuroendocrine systems. â J. Neuroendocrinol. 24: 144-159.
-
Gosling S.D. (2001). From mice to men: what can we learn about personality from animal research? â Psychol. Bull. 127: 45-86.
-
Guinn Sellers J., Mehl M.R., Josephs R.A. (2007). Hormones and personality: testosterone as a marker of individual differences. â J. Res. Person. 41: 126-138.
-
Jobling S., Nolan M., Tyler C.R., Brighty G., Sumpter J.P. (1998). Widespread sexual disruption in wild fish. â Environ. Sci. Technol. 32: 2498-2506.
-
Karino K., Someya C. (2007). The influence of sex, line, and fight experience on aggressiveness of the Siamese fighting dish in intrasexual competition. â Behav. Proc. 75: 283-289.
-
Kidd K.A., Blanchfield P.J., Mills K.H., Palace V.P., Evans R.E., Lazorchak J.M., Flick R.W. (2007). Collapse of a fish population after exposure to a synthetic estrogen. â Proc. Natl. Acad. Sci. USA 104: 8897-8901.
-
Kime D.E. (1998). Endocrine disruption in fish. â Kluwer, Boston, MA.
-
Kolpin D.W., Furlong E.T., Meyer M.T., Thurman E.M., Zaugg S.D., Barber L.B., Buxton H.T. (2002). Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999â2000: a national reconnaissance. â Environ. Sci. Technol. 36: 1202-1211.
-
Komers P.E. (2007). Behavioral plasticity in variable environments. â Can. J. Zool. 75: 161-169.
-
Kortet R., Hedrick A.V., Vainikka A. (2010). Parasitism, predation and the evolution of animal personalities. â Ecol. Lett. 13: 1449-1458.
-
Kristensen T., Baatrup E., Bayley M. (2005). 17α-ethinylestradiol reduces the competitive reproductive fitness of the male guppy (Poecilia reticulata). â Biol. Reprod. 72: 150-156.
-
Lai K.M., Scrimshaw M.D., Lester J.N. (2002). Prediction of the bioaccumulation factors and body burden of natural and synthetic estrogens in aquatic organisms in the river systems. â Sci. Total Environ. 289: 159-168.
-
Länge R., Hutchinson T.H., Croudace C.P., Siegmund F., Schweinfurth H., Hampe P., Panter G.H., Sumpter J.P. (2001). Effects of the synthetic oestrogen 17α-ethinyloestradiol on the life-cycle of the fathead minnow (Pimephales promelas). â Environ. Toxicol. Chem. 20: 1216-1227.
-
Larsen M.G., Hansen K.B., Henriksen P.G., Baatrup E. (2008). Male zebrafish (Danio rerio) courtship behaviour resists the feminizing effects of 17α-ethinyloestradiol â morphological sexual characteristics do not. â Aquat. Toxicol. 87: 234-244.
-
Larsson D.G.J., Adolfsson-Erici M., Parkkonen J., Pettersson M., Berg A.H., Olsson P.E., Forlin L. (1999). Ethinyloestradiol: an undesired fish contraceptive. â Aquat. Toxicol. 45: 91-97.
-
McCann K.S. (2000). The diversityâstability debate. â Nature 405: 228-233.
-
McNamara J.M., Barta Z., Fromhage L., Houston A.I. (2008). The coevolution of choosiness and cooperation. â Nature 451: 189-192.
-
Montgomery T.M., Brown A.C., Gendelman H.K., Ota M., Clotfelter E.D. (2012). Exposure to 17α-ethinylestradiol decreases motility and ATP in sperm of male fighting fish Betta splendens. â Environ. Toxicol., DOI:10.1002/tox.21752
-
Muller M., Rabenoelina F., Balaguer P., Patureau D., Lemenach K., Budzinski H., Barcelo D., De Alda M.L., Kuster M., Delgenes J.P., Hernandez-Raquet G. (2008). Chemical and biological analysis of endocrine-disrupting hormones and estrogenic activity in an advanced sewage treatment plant. â Environ. Toxicol. Chem. 27: 1649-1658.
-
Nakagawa S., Schielzeth H. (2010). Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. â Biol. Rev. 85: 935-956.
-
Nash J.P., Kime D.E., van der Ven L.T., Wester P.W., Brion F., Maack G., Stahlschmidt-Allner P., Tyler C.R. (2004). Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. â Environ. Health. Perspect. 112: 1725-1733.
-
Purdom C.E., Hardiman P.A., Bye V.J., Eno N.C., Tyler C.R., Sumpter J.P. (1994). Estrogenic effects of effluents from sewage treatment works. â Chem. Ecol. 8: 275-285.
-
Reale D., Reader S.M., Sol D., McDougall P.T., Dingemanse N.J. (2007). Integrating animal temperament within ecology and evolution. â Biol. Rev. 82: 291-318.
-
Rowland W.J. (1999). Studying visual cues in fish behavior: a review of ethological techniques. â Environ. Biol. Fish. 56: 285-305.
-
Saaristo M., Craft J.A., Lehtonen K.K., Lindstrom K. (2009). Sand goby (Pomatoschistus minutus) males exposed to an endocrine disrupting chemical fail in nest and mate competition. â Horm. Behav. 56: 315-321.
-
Saaristo M., Craft J.A., Lehtonen K.K., Lindstrom K. (2010). Exposure to 17α-ethinyl oestradiol impairs courtship and aggressive behaviour of male sand gobies (Pomatoschistus minutes). â Chemosphere 79: 541-546.
-
Salierno J.D., Kane A.S. (2009). 17α-ethinyloestradiol alters reproductive behaviours, circulating hormones, and sexual morphology in male fathead minnows (Pimephales promelas). â Environ. Toxicol. Chem. 28: 953-961.
-
Schuett W., Dall S.R.X. (2009). Sex differences, social context and personality in zebra finches, Taeniopygia guttata. â Anim. Behav. 77: 1041-1050.
-
Schuett W., Tregenza T., Dall S.R.X. (2010). Sexual selection and animal personality. â Biol. Rev. 85: 217-246.
-
Shenoy K., Crowley P.H. (2011). Endocrine disruption of male mating signals: ecological and evolutionary implications. â Funct. Ecol. 25: 433-448.
-
Shore L.S., Gurevitz M., Shemesh M. (1993). Estrogen as an environmental pollutant. â Bull. Environ. Contam. Toxicol. 51: 361-366.
-
Sih A. (2013). Frontiers on the interface between behavioral syndromes and social behavioral ecology. â In: Animal personalities: behavior, physiology, and evolution ( Carere C., Maestripieri D., eds). University of Chicago Press, Chicago, IL, p. 221-250.
-
Sih A., Bell A.M., Johnson J.C., Ziemba R.E. (2004). Behavioral syndromes: an integrative overview. â Q. Rev. Biol. 79: 241-277.
-
Sih A., Cote J., Evans M., Fogarty S., Pruitt J. (2012). Ecological implications of behavioral syndromes. â Ecol. Lett. 15: 278-289.
-
Sih A., Ferrari M.C.O., Harris D.J. (2011). Evolution and behavioral responses to human-induced rapid environmental change. â Evol. Appl. 4: 367-387.
-
Simpson M.J.A. (1968). The display of the Siamese fighting fish Betta splendens. â Anim. Behav. Monogr. 1: 1-73.
-
Smith B.R., Blumstein D.T. (2008). Fitness consequences of personality: a meta-analysis. â Behav. Ecol. 19: 448-455.
-
Stamps J.A., Groothuis T.G.G. (2010). The development of animal personality: relevance, concepts and perspectives. â Biol. Rev. 85: 301-325.
-
Stevenson L.M., Brown A.C., Montgomery T.M., Clotfelter E.D. (2011). Reproductive consequences of exposure to waterborne phytoestrogens in male fighting fish Betta splendens. â Arch. Environ. Contam. Toxicol. 60: 501-510.
-
Tyler C.R., Jobling S., Sumpter J.P. (1998). Endocrine disruption in wildlife: a critical review of the evidence. â Crit. Rev. Toxicol. 28: 319-361.
-
Zala S.M., Penn D.J. (2004). Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges. â Anim. Behav. 68: 649-664.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 561 | 45 | 13 |
| Full Text Views | 182 | 0 | 0 |
| PDF Views & Downloads | 31 | 0 | 0 |
Chronic exposure to 17α-ethinylestradiol reduces behavioral consistency in male Siamese fighting fish
In: BehaviourSearch for other papers by Teresa L. Dzieweczynski in
Current site
Google Scholar
PubMed
Search for other papers by Kimberly B. Hentz in
Current site
Google Scholar
PubMed
Search for other papers by Brittney Logan in
Current site
Google Scholar
PubMed
Search for other papers by Olivia L. Hebert in
Current site
Google Scholar
PubMed
Both acute and chronic exposure to 17α-ethinylestradiol (EE2), one of the primary active ingredients of birth control pills, decreases courtship and aggression in males of aquatic species. However, how exposure affects behavioral consistency over time is not commonly addressed. To examine the effects of chronic EE2 exposure on behavioral consistency, adult male Siamese fighting fish, Betta splendens, received multiple trials with a dummy male and dummy female presented simultaneously both before and after chronic exposure to a nominal dose (10 ng/l) of EE2. The responses of exposed males were compared before and after exposure and against those of a group of unexposed, control males. Male-directed and female-directed behaviors were reduced after 28 days of EE2 exposure. More importantly, chronic EE2 exposure had dramatic effects on consistent individual differences in female-directed and male-directed behaviors. Repeatability values were markedly lower and level of response was less correlated in the EE2 group, suggesting that exposure disrupts both between-individual variation and behavioral consistency. These results cannot be explained by a temporal effect as they were not found in the control group of unexposed males. This study demonstrates that EE2 exposure may have effects beyond a reduction in overall response. It also demonstrates the importance of studying the effects of chemical exposure on multiple time scales as acute exposure to EE2 affects the consistency of only female-directed behaviors in this species whereas chronic exposure affects consistency of both female-directed and male-directed behavior. Finally, this study suggests that males in this species may differ in their sensitivity, an important area for future research.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 561 | 45 | 13 |
| Full Text Views | 182 | 0 | 0 |
| PDF Views & Downloads | 31 | 0 | 0 |
