Abstract
Studies of aquatic environments exposed to 17α-ethinylestradiol (EE2) have demonstrated detrimental effects on fish communities. However, much less is known about effects on macro-invertebrates and especially how long-term exposure may affect critical life stages and ultimately population dynamics. We studied the effects of EE2 on relevant endpoints for population growth in two common freshwater gastropods, Radix balthica and Bithynia tentaculata, that differ in reproductive, foraging and anti-predator strategies and endocrine systems. We quantified critical life-history parameters (mortality, somatic growth rate, days to and size at first reproduction, egg production and hatching success) in a concentration–response, life cycle experiment. The two species responded to EE2 exposure in different ways, B. tentaculata showing a significantly lower somatic growth rate and R. balthica a higher somatic growth rate. However, the magnitudes of the effects were small and EE2 exposure did not have any significant effect on estimated population growth rates for the two snail species. The significant effects of EE2 on individual endpoints, but not on population growth rate for both species, emphasise the importance of evaluating higher level effects from long-term exposure studies.
Similar content being viewed by others
References
Andrew MN, Dunstan RH, O’Connor WA, Van Zwieten L, Nixon B, MacFarlane GR (2008) Effects of 4-nonylphenol and 17 alpha-ethynylestradiol exposure in the Sydney rock oyster, Saccostrea glomerata: vitellogenin induction and gonadal development. Aquat Toxicol 88(1):39–47. doi:10.1016/j.aquatox.2008.03.003
Beck I-C, Bruhn R, Gandrass J, Ruck W (2005) Liquid chromatography-tandem mass spectrometry analysis of estrogenic compounds in coastal surface water of the Baltic Sea. J Chromatogr A 1090(1–2):98–106
Bell AM (2004) An endocrine disrupter increases growth and risky behavior in three-spined stickleback (Gasterosteus aculeatus). Horm Behav 45(2):108–114. doi:10.1016/j.yhbeh.2003.09.009
Benstead RS, Baynes A, Casey D, Routledge EJ, Jobling S (2011) 17 beta-Oestradiol may prolong reproduction in seasonally breeding freshwater gastropod molluscs. Aquat Toxicol 101(2):326–334. doi:10.1016/j.aquatox.2010.11.005
Brendelberger H (1997) Contrasting feeding strategies of two freshwater gastropods, Radix peregra (Lymnaeidae) and Bithynia tentaculata (Bithyniidae). Arch Hydrobiol 140(1):1–21
Brian JV, Augley JJ, Braithwaite VA (2006) Endocrine disrupting effects on the nesting behaviour of male three-spined stickleback Gasterosteus aculeatus L. J Fish Biol 68(6):1883–1890
Cather JN, Verdonk NH (1974) Development of Bithynia-tentaculata (prosobranchia, gastropoda) after removal of polar lobe. J Embryol Exp Morphol 31:415–422
Czech P, Weber K, Dietrich DR (2001) Effects of endocrine modulating substances on reproduction in the hermaphroditic snail Lymnaea stagnalis L. Aquat Toxicol 53(2):103–114
Desbrow C, Routledge EJ, Brighty GC, Sumpter JP, Waldock M (1998) Identification of estrogenic chemicals in STW effluent 1 Chemical fractionation and in vitro biological screening. Environ Sci Technol 32(11):1549–1558
Dillon RT (2000) Gastropod autecology. In: Dillon RT (ed) The ecology of freshwater molluscs. Cambridge University Press, Cambridge, pp 54–114
Duft M, Schulte-Oehlmann U, Weltje L, Tillmann M, Oehlmann J (2003) Stimulated embryo production as a parameter of estrogenic exposure via sediments in the freshwater mudsnail Potamopyrgus antipodarum. Aquat Toxicol 64(4):437–449. doi:10.1016/S0166-445x(03)00102-4
Duft M, Schmitt C, Bachmann J, Brandelik C, Schulte-oehlmann U, Oehlmann J (2007) Prosobranch snails as test organisms for the assessment of endocrine active chemicals−an overview and a guideline proposal for a reproduction test with the freshwater mudsnail Potamopyrgus antipodarum. Ecotoxicology 16(1):169–182. doi:10.1007/s10646-006-0106-0
Forbes VE, Calow P (2002) Population growth rate as a basis for ecological risk assessment of toxic chemicals. Philos Trans R Soc Lond B 357(1425):1299–1306. doi:10.1098/rstb.2002.1129
Guillette LJ Jr, Crain DA, Rooney AA, Pickford DB (1995) Organization versus activation: The role of endocrine-disrupting contaminants (EDCs) during embryonic development in wildlife. Environ Health Perspect 103(SUPPL. 7):157–164
Hotchkiss AK, Rider CV, Blystone CR, Wilson VS, Hartig PC, Ankley GT, Foster PM, Gray CL, Gray LE (2008) Fifteen years after “Wingspread”−environmental endocrine disrupters and human and wildlife health: Where we are today and where we need to go. Toxicol Sci 105(2):235–259. doi:10.1093/toxsci/kfn030
Hutchinson TH, Shillabeer N, Winter MJ, Pickford DB (2006) Acute and chronic effects of carrier solvents in aquatic organisms: a critical review. Aquat Toxicol 76(1):69–92. doi:10.1016/j.aquatox.2005.09.008
Jobling S, Casey D, Rodgers-Gray T, Oehlmann J, Schulte-Oehlmann U, Pawlowski S, Baunbeck T, Turner AP, Tyler CR (2003) Comparative responses of molluscs and fish to environmental estrogens and an estrogenic effluent. Aquat Toxicol 65(2):205–220. doi:10.1016/S0166-445x(03)00134-6
Johnson AC, Aerni HR, Gerritsen A, Gibert M, Giger W, Hylland K, Juergens M, Nakari T, Pickering A, Suter MJF, Svenson A, Wettstein FE (2005) Comparing steroid estrogen, and nonylphenol content across a range of European sewage plants with different treatment and management practices. Water Res 39(1):47–58
Jokela J, Wiehn J, Kopp K (2006) Among-and within-population variation in outcrossing rate of a mixed-mating freshwater snail. Heredity 97(4):275–282
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(21):8897–8901. doi:10.1073/pnas.0609568104
Köhler H-R, Kloas W, Schirling M, Lutz I, Reye AL, Langen J-S, Triebskorn R, Nagel R, Schoenfelder G (2007) Sex steroid receptor evolution and signalling in aquatic invertebrates. Ecotoxicology 16(1):131–143. doi:10.1007/s10646-006-0111-3
Kuch HM, Ballschmiter K (2001) Determination of endocrine-disrupting phenolic compounds and estrogens in surface and drinking water by HRGC-(NCI)-MS in the picogram per liter range. Environ Sci Technol 35(15):3201–3206
Lafont R, Mathieu M (2007) Steroids in aquatic invertebrates. Ecotoxicology 16(1):109–130. doi:10.1007/s10646-006-0113-1
Lagadic L, Coutellec M-A, Caquet T (2007) Endocrine disruption in aquatic pulmonate molluscs: few evidences, many challenges. Ecotoxicology 16(1):45–59. doi:10.1007/s10646-006-0114-0
Langston WJ, Burt GR, Chesman BS (2007) Feminisation of male clams Scrobicularia plana from estuaries in Southwest UK and its induction by endocrine-disrupting chemicals. Mar Ecol Prog Ser 333:173–184
LeBlanc GA, McLachlan JB (1999) Molt-independent growth inhibition of Daphnia magna by a vertebrate antiandrogen. Environ Toxicol Chem 18(7):1450–1455. doi:10.1897/1551-5028(1999)018<1450:migiod>2.3.co;2
Matthiessen P (2008) An assessment of endocrine disruption in mollusks and the potential for developing internationally standardised mollusk life cycle test guidelines. Integr Environ Assess Manag 4(3):274–284
Matthiessen P, Gibbs PE (1998) Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environ Toxicol Chem 17(1):37–43
Nash JP, Kime DE, Van der Ven LTM, 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(17):1725–1733. doi:10.1289/Ehp.7209
Oehlmann J, Schulte-Oehlmann U (2003) Endocrine disruption in invertebrates. Pure Appl Chem 75(11–12):2207–2218. doi:10.1351/pac200375112207
Oehlmann J, Fioroni P, Stroben E, Markert B (1996) Tributyltin (TBT) effects on Ocinebrina aciculata (Gastropoda: Muricidae): imposex development, sterilization, sex change and population decline. Sci Total Environ 188(2–3):205–223
Oehlmann J, Schulte-Oehlmann U, Tillmann M, Markert B (2000) Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory Part I: bisphenol A and octylphenol as xeno-estrogens. Ecotoxicology 9(6):383–397
Oliveira-Filho EC, Grisolia CK, Roma Paumgartten FJ (2009) Effects of endosulfan and ethanol on the reproduction of the snail Biomphalaria tenagophila: a multigeneration study. Chemosphere 75(3):398–404. doi:10.1016/j.chemosphere.2008.11.085
Persson A, Svensson JM (2006) Effects of benthivorous fish on biogeochemical processes in lake sediments. Freshw Biol 51(7):1298–1309. doi:10.1111/j.1365-2427.2006.01569.x
Pojana G, Gomiero A, Jonkers N, Marcomini A (2007) Natural and synthetic endocrine disrupting compounds (EDCs) in water, sediment and biota of a coastal lagoon. Environ Int 33(7):929–936. doi:10.1016/j.envint.2007.05.003
Ricklefs RE (2001) Population Growth and Regulation. In: the economy of nature, 5th edn. Freeman and Company, New York, pp269-292
Schaefers C, Teigeler M, Wenzel A, Maack G, Fenske M, Segner H (2007) Concentration- and time-dependent effects of the synthetic estrogen, 17 alpha-ethinylestradiol, on reproductive capabilities of the zebrafish, Danio rerio. J Toxicol Environ Health A 70(9–10):768–779. doi:10.1080/15287390701236470
Schmitt C, Vogt C, Van Ballaer B, Brix R, Suetens A, Schmitt-Jansen M, De Deckere E (2010) In situ cage experiments with Potamopyrgus antipodarum−a novel tool for real life exposure assessment in freshwater ecosystems. Ecotoxicol Environ Saf 73(7):1574–1579. doi:10.1016/j.ecoenv.2010.07.014
Segner H, Caroll K, Fenske M, Janssen CR, Maack G, Pascoe D, Schaefers C, Vandenbergh GF, Watts M, Wenzel A (2003) Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project. Ecotoxicol Environ Saf 54(3):302–314
Shen JH, Gutendorf B, Vahl HH, Shen L, Westendorf J (2001) Toxicological profile of pollutants in surface water from an area in Taihu Lake, Yangtze Delta. Toxicology 166(1–2):71–78
Strong EE, Gargominy O, Ponder WF, Bouchet P (2008) Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. Hydrobiologia 595:149–166. doi:10.1007/s10750-007-9012-6
Tarrant AM, Atkinson MJ, Atkinson S (2004) Effects of steroidal estrogens on coral growth and reproduction. Mar Ecol Prog Ser 269:121–129. doi:10.3354/meps269121
Ternes TA, Stumpf M, Mueller J, Haberer K, Wilken RD, Servos M (1999) Behavior and occurrence of estrogens in municipal sewage treatment plants: I Investigations in Germany, Canada and Brazil. Sci Total Environ 225(1–2):81–90
Teske SS, Arnold RG (2008) Removal of natural and xeno-estrogens during conventional wastewater treatment. Rev Environ Sci Biotechnol 7(2):107–124. doi:10.1007/s11157-008-9129-8
Vanleeuwen CJ, Luttmer WJ, Griffioen PS (1985) The use of cohorts and populations in chronic toxicity studies with daphnia-magna−a cadmium example. Ecotoxicol Environ Saf 9(1):26–39
Walthall WK, Stark JD (1997) A comparison of acute mortality and population growth rate as endpoints of toxicological effect. Ecotoxicol Environ Saf 37(1):45–52
Watts MM, Pascoe D, Carroll K (2001) Survival and precopulatory behaviour of Gammarus pulex (L) exposed to two xenoestrogens. Water Res 35(10):2347–2352
Weltje L, vom Saal FS, Oehlmann J (2005) Reproductive stimulation by low doses of xenoestrogens contrasts with the view of hormesis as an adaptive response. Hum Exp Toxicol 24(9):431–437
WHO/IPCS (2002) In: Damastra T, Barlow S, Bergman A, Kavlock R, Van Der Kraak G (eds) Global assessment of the state-of-the-science of endocrine disruptors WHO/IPCS/EDC/022. World Health Organization, Geneva
Williams RJ, Johnson AC, Smith JJL, Kanda R (2003) Steroid estrogens profiles along river stretches arising from sewage treatment works discharges. Environ Sci Technol 37(9):1744–1750
Zorita S, Hallgren P, Mathiasson L (2008) Steroid hormone determination in water using an environmentally friendly membrane based extraction technique. J Chromatogr A 1192(1):1–8. doi:10.1016/j.chroma.2008.03.030
Acknowledgments
We thank Thomas Lakowitz for generously sharing his experience with gastropods. The study was supported by grants from the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS). We also thank the three anonymous reviewers for their valuable comments on an earlier version of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hallgren, P., Sorita, Z., Berglund, O. et al. Effects of 17α-ethinylestradiol on individual life-history parameters and estimated population growth rates of the freshwater gastropods Radix balthica and Bithynia tentaculata . Ecotoxicology 21, 803–810 (2012). https://doi.org/10.1007/s10646-011-0841-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-011-0841-8