Behavioral responses of adult male and female fathead minnows to a model estrogenic effluent and its effects on exposure regime and reproductive success

Aquatic Toxicology

Volumn 101, Issue 3-4, 2011, Pages 521-528

  Lavelle, Candice ^a   Sorensen, Peter W ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Behavior; Competitive mating; Environmental estrogen; Natural selection; Temperature

Indexed keywords

ESTROGEN;

BEHAVIORAL RESPONSE; CYPRINID; EFFLUENT; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; NATURAL SELECTION; POLLUTION EFFECT; POLLUTION EXPOSURE; REPRODUCTIVE SUCCESS;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EFFLUENT; ENVIRONMENTAL EXPOSURE; FEMALE; MALE; MAZE TEST; NONHUMAN; PIMEPHALES PROMELAS; PRIORITY JOURNAL; REPRODUCTION; SPAWNING; UNITED STATES; WASTE WATER TREATMENT PLANT; WATER POLLUTION; WATER TEMPERATURE;

ANIMALS; CYPRINIDAE; ENVIRONMENTAL EXPOSURE; ESTROGENS; FEMALE; MALE; MINNESOTA; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; STATISTICS, NONPARAMETRIC; TEMPERATURE; TIME FACTORS; VITELLOGENINS; WATER POLLUTANTS, CHEMICAL;

MISSISSIPPI RIVER; UNITED STATES;

CYPRINIDAE; PIMEPHALES PROMELAS; PISCES;

EID: 78651064821     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2010.12.007     Document Type: Article

References (37)

1. Andersen L., Holbech H., Gessbo A., Norrgren L., Petersen G.I. Effects of exposure to 17α-ethinylestradiol during early development on sexual differentiation and induction of vitellogenin in zebrafish (Danio rerio). Comp. Biochem. Physiol. C 2003, 134:365-374.
2. Balch G.C., Mackenzie C.A., Metcalfe C.D. Alterations to gonadal development and reproductive success in Japanese medaka (Oryzias latipes) exposed to 17α-ethinylestradiol. Environ. Toxicol. Chem. 2004, 23:782-791.
3. Barber L.B., Lee K.E., Swackhamer D.L., Schoenfuss H.L. Reproductive responses of male fathead minnows exposed to wastewater treatment plant effluent, effluent treated with XAD8 resin, and an environmentally relevant mixture of alkylphenol compounds. Aquat. Toxicol. 2007, 82:36-46.
4. Blair R.M., Fang H., Branham W.S., Hass B.S., Dial S.L., Moland C.L., Tong W.D., Shi L.M., Perkins R., Sheehan D.M. The estrogen receptor relative binding affinities of 188 natural and xenochemicals: structural diversity of ligands. Toxicol. Sci. 2000, 54:138-153.
5. Cheek A.O., Brouwer T.H., Carroll S., Manning S., McLachlan J.A., Brouwer M. Experimental evaluation of vitellogenin as a predictive biomarker for reproductive disruption. Environ. Health Perspect. 2001, 109:681-690.
6. Cherry D.S., Dickson K.L., Cairns J., Stauffer J.R. Preferred, avoided and lethal temperatures of fish during rising temperature conditions. J. Fish. Res. Board Can. 1977, 34:239-246.
7. Colborn T., vom Saal F.S., Soto A.M. Developmental effects of endocrine disrupting chemicals in wildlife and humans. Environ. Health Perspect. 1993, 101:1096-1100.
8. Colman J.R., Baldwin D.H., Johnson L.L., Scholz N.L. Effects of the synthetic estrogen, 17α-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). Aquat. Toxicol. 2009, 91:346-354.
9. Cooke S.J., Bunt C.M., Schreer J.F. Understanding fish behavior, distribution, and survival in thermal effluents using fixed telemetry arrays: a case study of smallmouth bass in a discharge canal during winter. Environ. Manage. 2004, 33:140-150.
10. Cooke S.J., McKinley S. Winter residency and activity patterns of channel catfish, Ictalurus punctatus (Rafinesque), and common carp, Cyprinus carpio L., in a thermal discharge canal. Fish. Manage. Ecol. 1999, 6:515-526.
11. Danylchuk A.J., Tonn W.M. Effects of social structure on reproductive activity in male fathead minnow. Behav. Ecol. 2001, 4:482-489.
12. Fava J.A., Tsai C.-F. Immediate behavioral reactions of blacknose dace, Rhinichthys atratulus, to domestic sewage and its toxic constituents. Trans. Am. Fish. Soc. 1976, 105:430-441.
13. Folmar L.C., Denslow N.D., Rao V., Chow M., Crain D.A., Enblom J., Marcino J., Guillette L.J. Vitellogenin induction and reduced serum testosterone concentrations in wild male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environ. Health Perspect. 1996, 104:1096-1101.
14. Folmar L.C., Denslow N.D., Kroll K., Orlando E.F., Enblom J., Marcino J., Metcalfe C., Guillette J.R.L.J. Altered sex serum steroids and vitellogenin induction in walleye (Stizostedion vitreum) collected near a metropolitan sewage treatment plant. Arch. Environ. Contam. Toxicol. 2001, 40:392-398.
15. Garcia-Reyero N., Lavelle C., Escalon B.L., Martinovic D., Sorensen P.W., Denslow N.D. Overview of the effluent water effects on the fathead minnow. Aquat. Toxicol. 2011, 101:38-48.
16. Hazel J. Thermal biology. Fish Physiology 1993, CRC Press, Tampa, FL, pp. 427-468. D.H. Evans (Ed.).
17. Isaac D., 1961. The ecological life history of the fathead minnow, Pimephales promelas (Rafinesque). Unpublished Ph.D. dissertation, University of Minnesota, Minneapolis, MN.
18. Kolpin D.W., Furlong E.T., Meyer M.T., Thurman E.M., Zaugg S.D., Barber L.B., Buxton H.T. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a national reconnaissance. Environ. Sci. Technol. 2002, 36:1202-1211.
19. Korte J.J., Kahl M.D., Jensen K.M., Pasha M.S., Parks L.G., LeBlanc G.A., Ankley G.T. Fathead minnow vitellogenin: complementary DNA sequence and messenger RNA and protein expression after 17β-estradiol treatment. Environ. Toxicol. Chem. 2000, 19:972-981.
20. Lange R., Hutchinson T.H., Croudace C.P., Siegmund F., Schweinfurth H., Hampe P., Panter G.H., Sumpter J.P. Effects of the synthetic estrogen 17R-ethinylestradiol over the life-cycle of the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 2001, 20:1216-1227.
21. Lee, K.E., Barber, L.B., Furlong, E.T., Cahill, J.D., Kopin, D.W., Meyer, M.T., Zaugg, S.D., 2004. Presence and distribution or organic wastewater compounds in wastewater, surface, ground, and drinking waters, Minnesota, 2000-02. Scientific Investigation Report 2004-5138. USGS, Reston, Virginia.
22. Liley N.R. The effects of estrogens and other steroids on the sexual behavior of the female guppy Poecilia reticulate. Gen. Comp. Endocrinol. Suppl. 1972, 3:542-552.
23. Martinović D., Hogarth W.T., Jones R.E., Sorensen P.W. Environmental estrogens suppress hormones, behavior, and reproductive fitness in male fathead minnows. Environ. Toxicol. Chem. 2007, 26:271-278.
24. Martinović D., Denny J.S., Schmeider P.K., Ankley G.T., Sorensen P.W. Temporal variation in the estrogenicities of a sewage treatment plant effluent and its biological significance. Environ. Sci. Technol. 2008, 42:3421-3427.
25. McGee M., Julius M.L., Vajda A.M., Norris D.O., Barber L.B., Schoenfuss H.L. Predator avoidance of larval fathead minnows (Pimephales promelas) following short-term exposure to estrogen mixtures. Aquat. Toxicol. 2009, 91:355-361.
26. Metcalfe C.D., Metcalfe T.L., Kiparissis Y., Koenig B.G., Khan C., Hughes R.J., Croley T.R., March R.E., Potter T. Estrogenic potency of chemicals detected in sewage treatment plant effluents as determined by in vivo assays with Japanese medaka (Oryzias latipes). Environ. Toxicol. Chem. 2001, 20:297-308.
27. Mills L.J., Chichester C. Review of evidence: are endocrine-disrupting chemicals in the aquatic environment impacting fish populations?. Sci. Total Environ. 2005, 343:1-34.
28. Panter G.H., Thompson R.S., Sumpter J.P. Adverse reproductive effects in male fathead minnows (Pimephales promelas) exposed to environmentally relevant concentrations of the natural oestrogens, oestradiol and oestrone. Aquat. Toxicol. 1998, 42:243-253.
29. Schoenfuss H.L., Levitt J.T., Van Der Kraak G., Sorensen P.W. Ten week exposure to treated sewage discharge has relatively minor, variable effects on reproductive behavior and sperm production in goldfish. Environ. Toxicol. Chem. 2002, 21:2185-2190.
30. Schoenfuss H.L., Bartell S.E., Bistodeau T.B., Cediel R.A., Grove K.J., Zintek L., Lee K.E., Barber L.B. Impairment of the reproductive potential of male fathead minnows by environmentally relevant exposures to 4-nonylphenol. Aquat. Toxicol. 2008, 86:91-98.
31. Segner H., Caroll K., Fenske M., Janssen C.R., Maack G., Pascoe D., Schäfers C., Vandenbergh G.F., Watts M., Wenzel A. Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project. Ecotoxicol. Environ. Saf. 2003, 54:302-314.
32. Sonnenschein C., Soto A.M. An updated review of environmental estrogen and androgen mimics and antagonists. Steriod Biochem. Mol. Biol. 1998, 65:143-150.
33. Sorensen P.W., Caprio J. Chemoreception in fish. The Physiology of Fishes 1998, CRC Press, FL, pp. 375-406. 2nd ed. D.E. Evans (Ed.).
34. Stacey N.E., Sorensen P.W. Hormonal pheromones in fish. Hormones, Brain and Behavior 2009, Elsevier Press, San Diego, pp. 638-661. 2nd ed. D.W. Pfaff, A.P. Arnold, A. Etgen, S. Fahrbach, R. Rubin (Eds.).
35. Sumpter J.P., Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health Perspect. 1995, 103:173-178.
36. Tyler C.R., Routledge E.J., van Aerle R. Estrogenic effects of treated sewage effluent on fish: steroids and surfactants in English rivers. The Toxicology of Fishes 2008, Taylor & Francis, Boca Raton, FL, pp. 971-1002. R.T. Di Giulio, D.E. Hinton (Eds.).
37. Wisenden B.D., Chivers P.D., Brown G.E., Smith R.J.F. The role of experience in risk assessment: avoidance of areas chemically labeled with fathead minnow alarm pheromone by conspecifics and heterospecifics. Ecoscience 1995, 2:116-122.