17β-Oestradiol may prolong reproduction in seasonally breeding freshwater gastropod molluscs

Aquatic Toxicology

Volumn 101, Issue 2, 2011, Pages 326-334

  Benstead, Rachel S ^a,b   Baynes, Alice ^b   Casey, Daire ^a   Routledge, Edwin J ^b   Jobling, Susan ^b  

^a ENVIRONMENT AGENCY   (United Kingdom)

^b BRUNEL UNIVERSITY   (United Kingdom)

Author keywords

Endocrine disruption; Mesocosm exposure; Planorbarius corneus; Seasonal reproduction; Steroid effects; Viviparus viviparus

Indexed keywords

ESTRADIOL;

ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; GASTROPOD; MATURATION; MESOCOSM; MORTALITY; PHOTOPERIOD; REPRODUCTION; REPRODUCTIVE BEHAVIOR; SNAIL; SPAWNING; STEROID; TEMPERATURE EFFECT;

AQUATIC ENVIRONMENT; ARTICLE; AUTUMN; CONTROLLED STUDY; EGG LAYING; ENVIRONMENTAL EXPOSURE; GASTROPOD; MESOCOSM; MORTALITY; NONHUMAN; PLANORBARIUS CORNEUS; PRIORITY JOURNAL; REPRODUCTION; SEASONAL VARIATION; SUMMER; TEMPERATURE; VIVIPARUS VIVIPARUS; WATER ANALYSIS; WATER QUALITY;

ANIMALS; ESTRADIOL; GASTROPODA; PHOTOPERIOD; REPRODUCTION; SEASONS; TEMPERATURE; WATER POLLUTANTS, CHEMICAL;

GASTROPODA; INVERTEBRATA; MOLLUSCA; PLANORBARIUS CORNEUS; VIVIPARUS VIVIPARUS;

EID: 78649922983     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2010.11.005     Document Type: Article

References (41)

1. Aufderheide J., Warbritton R., Pounds N., File-Emperador S., Staples C., Caspers N., Forbes V. Effects of husbandry parameters on the life-history traits of the apple snail Marisa cornuarietis: effects of temperature, photoperiod and population density. Invertebr. Biol. 2006, 125:9-20.
2. Bohlken S., Joosse J. The effect of photoperiod on female reproductive activity of the freshwater pulmonate snail Lymnaea stagnalis kept under laboratory breeding conditions. Int. J. Invertebr. Reprod. 1982, 4:213-222.
3. Calow P. The evolution of life-cycle strategies in fresh-water gastropods. Malacologia 1978, 17:351-364.
4. Canesi L., Ciacci C., Betti M., Lorusso L.C., Marchi B., Burattini S., Falcieri E., Gallo G. Rapid effects of 17β-estradiol on cell signalling and function of Mytilus hemocytes. Gen. Comp. Endocrinol. 2004, 136:58-71.
5. Ciocan C.M., Cubero-Leon E., Puinean A.M., Hill E.M., Minier C., Osada M., Fenlon K., Rotchell J.M. Effects of estrogen exposure in mussels, Mytilus edulis, at different stages of gametogenesis. Environ. Pollut. 2010, 158:2977-2984.
6. Clarke N., Routledge E.J., Garner A., Casey D., Benstead R., Walker D., Watermann B., Knass B., Tomsen A., Jobling S. Exposure to treated sewage effluent disrupts reproduction and development in the seasonally breeding ramshorn snail (Subclass: Pulmonata, Planorbarius corneus). Environ. Sci. Technol. 2009, 43:2092-2098.
7. Costil K. Influence of temperature on survival and growth of two freshwater Planorbid species, Planorbarius corneus (L.) and Planorbis planorbis (L.). J. Mollus. Stud. 1994, 60:223-235.
8. Costil K., Daguzan J. Effect of temperature on reproduction in Planorbarius corneus (L.) and Planorbis planorbis (L.) throughout the life span. Malacologia 1995, 36(1-2):79-89.
9. Croll R.P., Wang C. Possible roles of sex steroids in the control of reproduction in bivalve molluscs. Aquaculture 2007, 272:76-86.
10. Cubero-Leon E., Ciocan C.M., Hill E.M., Osada M., Kishida M., Itoh N., Kondo R., Minier C., Rotchell J.M. Estrogens disrupt serotonin receptor and cyclooxygenase mRNA expression in the gonads of mussels (Mytilus edulis). Aquat. Toxicol. 2010, 98:178-187.
11. Dogterom G.E., Thijssen R., van Lounhout H. Environmental and hormonal control of the seasonal egg laying period in field specimens of Lymnaea stagnalis. Gen. Comp. Endocrinol. 1985, 57:37-42.
12. Forbes V.E., Aufderheide J., Warbritton R., van der Hoeven N., Caspers N. Does Bisphenol A induce superfeminization in Marisa cornuarietis? Part II. Toxicity test results and requirements for statistical power analysis. Ecotoxicol. Environ. Saf. 2007, 66:319-325.
13. Forbes V.E., Selck H., Palmqvist A., Aufderheide J., Warbritton R., Pounds N., Thompson R., ver der Hoeven N., Caspers N. Does Bisphenol A induce superfeminization in Marisa cornuarietis? Part I. Intra- and inter-laboratory variability in test endpoints. Ecotoxicol. Environ. Saf. 2007, 66:309-318.
14. Geraerts W.P.M., Joosse J. Control of vitellogenesis and of growth of female accessory sex organs by the dorsal body hormone (DBH) in the hermaphroditic freshwater snail Lymnaea stagnalis. Gen. Comp. Endocrinol. 1975, 27:450-464.
15. Harries J.E., Runnalls T., Hill E., Harris C.A., Maddix S., Sumpter J.P., Tyler C.R. Development of a reproductive performance test for endocrine disrupting chemicals using pair-breeding fathead minnows (Pimephales promelas). Environ. Sci. Technol. 2000, 34:3003-3011.
16. Jobling S., Beresford N., Nolan M., Rodgers-Gray T., Brighty G.C., Sumpter J.P., Tyler C.R. Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluent. Biol. Reprod. 2002, 66:272-281.
17. Jobling S., Coey S., Whitmore J.G., Kime D.E., Van Look K.J.W., McAllister B.G., Beresford N., Henshaw A.C., Brighty G., Tyler C.R., Sumpter J.P. Wild intersex roach (Rutilus rutilus) have reduced fertility. Biol. Reprod. 2002, 67:515-524.
18. Jobling S., Casey D., Rodgers-Gray T., Oehlmann J., Schulte-Oehlmann U., Pawlowski S., Baunbeck T., Turner A.P., Tyler C.R. Comparative responses of molluscs and fish to environmental estrogens and an estrogenic effluent. Aquat. Toxicol. 2004, 66:207-222.
19. Kadam P.A., Kadam A.L., Segal S.J., Koide S.S. Functional serotonin receptor sites on Atlantic surf clam Spisula solidissima (Dillwyn, 1817) oocytes and sperm. J. Shellfish Res. 1991, 10:215-219.
20. Kajiwara M., Kuraku S., Kurakawa T., Kato K., Toda S., Hirose H., Takahashi S., Shibata Y., Iguchi T., Matsumoto T., Miyata T., Miura T., Takahashi Y. Tissue preferential expression of estrogen receptor gene in the marine snail Thais clavigera. Gen. Comp. Endocrinol. 2006, 148:315-326.
21. Katsu Y., Lange A., Urushitani H., Ichikawa R., Paull G., Cahill L., Jobling S., Tyler C., Iguchi T. Functional associations between two estrogen receptors, environmental estrogens, and sexual disruption in the roach (Rutilus rutilus). Environ. Sci. Technol. 2007, 41:3368-3374.
22. Keay J., Bridgham J.T., Thornton J.W. The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications. Endocrinology 2006, 147:3861-3869.
23. Manger P., Li J., Christensen B.M., Yoshito T.P. Biogenic monoamines in the freshwater snail, Biomphalaria glabrata: influence of infection by the human blood fluke, Schistosoma mansoni. Comp. Biochem. Physiol. 1996, 114A:227-234.
24. Mori K. Effect of steroid on oyster. IV. Acceleration of sexual maturation in female Crassotrea gigas by estradiol-17β. Bull. Jpn. Soc. Sci. Fish. 1969, 35:1077-1079.
25. Muschamp J.W., Fong P.P. Effects of the serotonin receptor ligand methiothepin on reproductive behaviour of the freshwater snail Biomphalaria glabrata: reduction of egg laying and induction of penile erection. J. Exp. Zool. 2001, 289:202-207.
26. Oehlmann J., Schulte-Oehlmann U., Tillmann M., Markert B. Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part 1. Bisphenol A and octylphenol as xeno-estrogens. Ecotoxicology 2000, 9:383-397.
27. Oehlmann J., Schulte-Oehlmann U., Bachmann J., Oetken M., Lutz I., Kloas W., Ternes T.A. Bisphenol A induces superfeminization in the ramshorn snail Marisa cornuarietis (Gastropoda: Prosobranchia) at environmentally relevant concentrations. Environ. Health Perspect. 2006, 114:127-133.
28. Oehlmann J., Di Benedetto P., Tillmann M., Duft M., Oetken M., Schulte-Oehlmann U. Endocrine disruption in prosobranch molluscs: evidence and ecological relevance. Ecotoxicology 2007, 16:29-43.
29. Oehlmann J., Oetken M., Schulte-Oehlmann U. A critical evaluation of the environmental risk assessment for plasticizers in the freshwater environment in Europe, with special emphasis on Bisphenol A and endocrine disruption. Environ. Res. 2008, 108:140-149.
30. Osada M., Mori K., Nomura T. In vitro effects of estrogen and serotonin on release of eggs from the ovary of the scallop. Nippon Suisan Gakkai Shi 1992, 58:223-227.
31. Osada M., Nakata A., Matsumoto T., Mori K. Pharmacological characterization of seratonin receptor in the oocyte membrane of bivalve molluscs and its formation during oogenesis. J. Exp. Zool. 1998, 281:124-131.
32. Reis-Henriques M.A., Le Guellec D., Remy-Martin J.P., Adessi G.L. Studies of endogenous steroids from the marine mollusc Mytilus edulis L. by gas chromatography and mass spectrometry. Comp. Biochem. Physiol. 1990, 95B:303-309.
33. Rodgers-Gray T.P., Jobling S., Kelly C., Morris S., Brighty G., Waldock M.J., Sumpter J.P., Tyler C.R. Exposure of juvenile roach (Rutilus rutilus) to treated sewage effluent induces dose-dependent and persistent disruption in gonadal duct development. Environ. Sci. Technol. 2001, 35:462-470.
34. Selck H., Aufderheide J., Pounds N., Staples C., Caspers N., Forbes V. Effects of food type, feeding frequency, and temperature on juvenile survival and growth of Marisa cornuarietis (Mollusca: Gastropoda). Invertebr. Biol. 2006, 125(2):106-116.
35. Sohoni P., Tyler C.R., Hurd K., Caunter J., Hetheridge M., Williams T., Woods C., Evans M., Toy R., Gargas M., Sumpter J.P. Reproductive effects of long-term exposure to Bisphenol A in the fathead minnow (Pimephales promelas). Environ. Sci. Technol. 2001, 35:2917-2925.
36. Sugamori K.S., Sunahara R.K., Guan H., Bulloch A.G.M., Tensen C.P., Seeman P., Niznik H.B., van Tol H.H.M. Seratonin receptor cDNA cloned from Lymnaea stagnalis. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:11-15.
37. Sumpter J.P., Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health Perspect. 1995, 103:173-178.
38. ter Maat A., Lodder J.C., Wilbrink M. Induction of egg laying in the pond snail Lymnaea stagnalis by environmental stimulation of the release of ovulation hormone from the caudo-dorsal cells. Int. J. Invertebr. Reprod. 1983, 6:239-247.
39. Thornton J.W., Need E., Crews D. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signalling. Science 2001, 301:1714-1717.
40. Wang C., Croll R.P. Effects of sex steroids on spawning in the sea scallop Placopecten megellanicus. Aquaculture 2006, 256:423-432.
41. Wayne N.L. Regulation of seasonal reproduction in mollusks. J. Biol. Rhythms 2001, 16(4):391-402.