[en] Alterations of the reproductive organs of gastropod molluscs exposed to pollutants have been reported in natural populations for more than 40 years. In some cases these impacts have been linked to exposure to endocrine disrupting chemicals (EDCs), which are known to induce adverse impacts on vertebrates, mainly by direct binding to steroid receptors or by altering hormone synthesis. Investigations on the mechanisms of action of endocrine disruptors in molluscs show that EDCs induce modifications of endogenous titres of androgens (e.g., testosterone, androstenedione) and oestrogens (e.g., 17ß-oestradiol). Alterations of the activity of enzymes related to steroid metabolism (i.e., cytochrome P450 aromatase, acyltransferases) are also often observed. In bivalves and gastropods, fatty acid esterification of steroids might constitute the major regulation of androgen and oestrogen homeostasis. The present review indicates that metabolism of steroid hormones to fatty acid esters might be a target of synthetic EDCs. Alterations of this process would impact the concentrations of free, potentially bioactive, form of steroids.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Giusti, Arnaud ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie animale et écotoxicologie
Joaquim-Justo, Célia ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie animale et écotoxicologie
Language :
English
Title :
Esterification of vertebrate like steroids in molluscs: A target of endocrine disruptors?
Publication date :
November 2013
Journal title :
Comparative Biochemistry and Physiology. C, Comparative Pharmacology and Toxicology
S. Abidli, M.M. Santos, Y. Lahbib, L.F.C. Castro, M.A. Reis-Henriques, and N. Trigui El Menif Tributyltin (TBT) effects on Hexaplex trunculus and Bolinus brandaris (Gastropoda: Muricidae): imposex induction and sex hormone levels insights Ecol. Indic. 13 2012 13 21
M.N. Andrew-Priestley, W.A. O'Connor, R.H. Dunstan, L. Van Zwieten, T. Tyler, A. Kumar, and G.R. MacFarlane Estrogen mediated effects in the Sydney rock oyster, Saccostrea glomerata, following field exposures to sewage effluent containing estrogenic compounds and activity Aquat. Toxicol. 120-121 2012 99 108
C.M. Barroso, M.A. Reis-Henriques, M. Ferreira, P.E. Gibbs, and M.H. Moreira Organotin contamination, imposex and androgen/oestrogen ratios in natural populations of Nassarius reticulatus along a ship density gradient Appl. Organomet. Chem. 19 2005 1141 1148 (Pubitemid 41560558)
B. Bauer, P. Fioroni, U. Schulte-Oehlmann, J. Oehlmann, and W. Kalbfus The use of Littorina littorea for tributyltin (TBT) effect monitoring - results from the German TBT survey 1994/1995 and laboratory experiments Environ. Pollut. 96 1997 299 309 (Pubitemid 27390440)
V. Bellet, G. Hernandez-Raquet, S. Dagnino, L. Seree, P. Pardon, C. Bancon-Montiny, H. Fenet, N. Creusot, S. Aït-Aïssa, V. Cavailles, H. Budzinski, J.-P. Antignac, and P. Balaguer Occurrence of androgens in sewage treatment plants influents is associated with antagonist activities on other steroid receptors Water Res. 46 2012 1912 1922
R.S. Benstead, A. Baynes, D. Casey, E.J. Routledge, and S. Jobling 17β-Oestradiol may prolong reproduction in seasonally breeding freshwater gastropod molluscs Aquat. Toxicol. 101 2011 326 334
C. Bettin, J. Oehlmann, and E. Stroben TBT-induced imposex in marine neogastropods is mediated by an increasing androgen level Helgoländer Meeresun. 50 1996 299 317 (Pubitemid 126729682)
S.J.M. Blaber The occurence of a penis-like outgrowth behind the right tentacle in spent females of Nucella lapillus (L.) J. Molluscan Stud. 39 1970 231 233
L.F.C. Castro, D. Lima, A. Machado, C. Melo, Y. Hiromori, J. Nishikawa, T. Nakanishi, M.A. Reis-Henriques, and M.M. Santos Imposex induction is mediated through the retinoid X receptor signalling pathway in the neogastropod Nucella lapillus Aquat. Toxicol. 85 2007 57 66 (Pubitemid 47419050)
T.-S. Chen, T.-C. Chen, K.-Y.C. Yeh, H.-R. Chao, E.-T. Liaw, C.-Y. Hsieh, K.-C. Chen, L.-T. Hsieh, and Y.-L. Yeh High estrogen concentrations in receiving river discharge from a concentrated livestock feedlot Sci. Total. Environ. 408 2010 3223 3230
D. De Longcamp, P. Lubet, and M. Drosdowsky The in vitro biosynthesis of steroids by the gonad of the mussel (Mytilus edulis) Gen. Comp. Endocrinol. 22 1974 116 127
A.M. De Souza, and D.N. De Oliveira Esterification of cholesterol and cholesterol ester hydrolysis by the hemolymph of the mollusc Biomphalaria Glabrata Comp. Biochem. Physiol. B 53 1976 345 347
A. Di Cosmo, C. Di Cristo, and M.a Paolucci Sex steroid hormone fluctuations and morphological changes of the reproductive system of the female of Octopus vulgaris throughout the annual cycle J. Exp. Zool. 289 2001 33 47 (Pubitemid 32100490)
M. Duft, U. Schulte-Oehlmann, L. Weltje, M. Tillmann, and J. Oehlmann Stimulated embryo production as a parameter of estrogenic exposure via sediments in the freshwater mudsnail Potamopyrgus antipodarum Aquat. Toxicol. 64 2003 437 449 (Pubitemid 36876122)
D. Fernandes, J.C. Navarro, C. Riva, S. Bordonali, and C. Porte Does exposure to testosterone significantly alter endogenous metabolism in the marine mussel Mytilus galloprovincialis? Aquat. Toxicol. 100 2010 313 320
D. Fernandes, B. Loi, and C. Porte Biosynthesis and metabolism of steroids in molluscs J. Steroid Biochem. Mol. Biol. 127 2011 189 195
F. Gagné, C. Blaise, J. Pellerin, and S. Gauthier-Clerc Alteration of the biochemical properties of female gonads and vitellins in the clam Mya arenaria at contaminated sites in the Saguenay Fjord Mar. Environ. Res. 53 2002 295 310 (Pubitemid 34037055)
F. Gagné, B. Bouchard, C. André, E. Farcy, and M. Fournier Evidence of feminization in wild Elliptio complanata mussels in the receiving waters downstream of a municipal effluent outfall Comp. Biochem. Physiol. C 153 2011 99 106
S. Gauthier-Clerc, J. Pellerin, and J.C. Amiard Estradiol-17ß and testosterone concentrations in male and female Mya arenaria (Mollusca bivalvia) during the reproductive cycle Gen. Comp. Endocrinol. 145 2006 133 139 (Pubitemid 43005047)
A. Giusti, V. Ducrot, C. Joaquim-Justo, and L. Lagadic Testosterone levels and fecundity in the hermaphroditic aquatic snail Lymnaea stagnalis exposed to testosterone and endocrine disruptors Environ. Toxicol. Chem. 32 2013 1740 1745
M.P. Gooding, and G.d.A LeBlanc Biotransformation and disposition of testosterone in the eastern mud snail Ilyanassa obsoleta Gen. Comp. Endocrinol. 122 2001 172 180 (Pubitemid 32424193)
M.P. Gooding, and G.A. LeBlanc Seasonal variation in the regulation of testosterone levels in the eastern mud snail (Ilyanassa obsoleta) Invertebr. Biol. 123 2004 237 243 (Pubitemid 39474460)
M.P. Gooding, V.S. Wilson, L.C. Folmar, D.T. Marcovich, and G.A. LeBlanc The biocide tributyltin reduces the accumulation of testosterone as fatty acid esters in the mud snail (Ilyanassa obsoleta) Environ. Health Perspect. 111 2003
H. Gottfried, and R.I. Dorfman Steroids of invertebrates V. The in vitro biosynthesis of steroids by the male-phase ovotestis of the slug (Ariolimax californicus) Gen. Comp. Endocrinol. 15 1970 120 138
M. Gust, T. Buronfosse, L. Giamberini, M. Ramil, R. Mons, and J. Garric Effects of fluoxetine on the reproduction of two prosobranch mollusks: Potamopyrgus antipodarum and Valvata piscinalis Environ. Pollut. 157 2009 423 429
M. Gust, T. Buronfosse, O. Geffard, R. Mons, H. Queau, J. Mouthon, and J. Garric In situ biomonitoring of freshwater quality using the New Zealand mudsnail Potamopyrgus antipodarum (Gray) exposed to waste water treatment plant (WWTP) effluent discharges Water Res. 44 2010 4517 4528
M. Gust, J. Mouthon, H. Queau, C. Dussart, T. Buronfosse, and J. Garric Natural variability and response interpretation of fecundity, vertebrate-like sex-steroid levels and energy status in the New Zealand mudsnail Potamopyrgus antipodarum (Gray) Gen. Comp. Endocrinol. 172 2011 243 250
T. Horiguchi, J.-H. Lee, J.-C. Park, H.-S. Cho, H. Shiraishi, and M. Morita Specific accumulation of organotin compounds in tissues of the rock shell, Thais clavigera Mar. Environ. Res. 76 2012 56 62
IPCS, I.P.o.C.S. Tributyltin compounds W.H. Organisation International Programme on Chemical Safety (Environmental Health Criteria 116) 1990 World Health Organisation Geneva
IPCS, I.P.o.C.S. Global Assessment of the State-of-the-Science of Endocrine Diruptors W.H.O. (WHO) International Program on Chemical Safety 2002
M.O. James Steroid catabolism in marine and freshwater fish J. Steroid Biochem. Mol. Biol. 127 2011 167 175
G. Janer, S. Mesia-Vela, C. Porte, and F.C. Kauffman Esterification of vertebrate-type steroids in the Eastern oyster (Crassostrea virginica) Steroids 69 2004 129 136 (Pubitemid 38315086)
G. Janer, R. Lavado, R. Thibaut, and C. Porte Effects of 17β-estradiol exposure in the mussel Mytilus galloprovincialis: a possible regulating role for steroid acyltransferases Aquat. Toxicol. 75 2005 32 42 (Pubitemid 41316974)
G. Janer, G.A. LeBlanc, and C. Porte A comparative study on androgen metabolism in three invertebrate species Gen. Comp. Endocrinol. 143 2005 211 221 (Pubitemid 41160440)
G. Janer, R.M. Sternberg, G.A. LeBlanc, and C. Porte Testosterone conjugating activities in invertebrates: are they targets for endocrine disruptors? Aquat. Toxicol. 71 2005 273 282 (Pubitemid 40164494)
G. Janer, A. Lyssimachou, J. Bachmann, J. Oehlmann, U. Schulte-Oehlmann, and C. Porte Sexual dimorphism in esterified steroid levels in the gastropod Marisa cornuarietis: the effect of xenoandrogenic compounds Steroids 71 2006 435 444
R. Jeannot, H. Sabik, E. Sauvard, T. Dagnac, and K. Dohrendorf Determination of endocrine-disrupting compounds in environmental samples using gas and liquid chromatography with mass spectrometry J. Chromatogr. A 974 2002 143 159
M. Kajiwara, S. Kuraku, T. Kurokawa, K. Kato, S. Toda, H. Hirose, S. Takahashi, Y. Shibata, T. Iguchi, T. Matsumoto, T. Miyata, T. Miura, and Y. Takahashi Tissue preferential expression of estrogen receptor gene in the marine snail, Thais clavigera Gen. Comp. Endocrinol. 148 2006 315 326 (Pubitemid 44286864)
J. Keay, J.T. Bridgham, and J.W. Thornton The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications Endocrinology 147 2006 3861 3869 (Pubitemid 44079391)
I. Ketata, F. Guermazi, T. Rebai, and A. Hamza-Chaffai Variation of steroid concentrations during the reproductive cycle of the clam Ruditapes decussatus: a one year study in the gulf of Gabès area Comp. Biochem. Physiol. A 147 2007 424 431 (Pubitemid 46629147)
H.-R. Köhler, W. Kloas, M. Schirling, I. Lutz, A. Reye, J.-S. Langen, R. Triebskorn, R. Nagel, and G. Schönfelder Sex steroid receptor evolution and signalling in aquatic invertebrates Ecotoxicology 16 2007 131 143
E.P. Kolodziej, J.L. Gray, and D.L. Sedlak Quantification of steroid hormones with pheromonal properties in municipal wastewater effluent Environ. Toxicol. Chem. 22 2003 2622 2629 (Pubitemid 37214746)
K.O. Kusk, T. Krüger, M. Long, C. Taxvig, A.E. Lykkesfeldt, H. Frederiksen, A.-M. Andersson, H.R. Andersen, K.M.S. Hansen, C. Nellemann, and E.C. Bonefeld-Jørgensen Endocrine potency of wastewater: contents of endocrine disrupting chemicals and effects measured by in vivo and in vitro assays Environ. Toxicol. Chem. 30 2011 413 426
P. Labadie, M.R. Peck, C. Minier, and E.M. Hill Identification of the steroid fatty acid ester conjugates formed in vivo in Mytilus edulis as a result of exposure to estrogens Steroids 72 2007 41 49 (Pubitemid 46037760)
R. Lafont, and M. Mathieu Steroids in aquatic invertebrates Ecotoxicology 16 2007 109 130 (Pubitemid 46292044)
R. Lavado, G. Janer, and C. Porte Steroid levels and steroid metabolism in the Mussel Mytilus edulis: the modulating effect of dispersed crude oil and alkylphenols Aquat. Toxicol. 78 2006 S65 S72
R. Lazzara, M. Blázquez, C. Porte, and C. Barata Low environmental levels of fluoxetine induce spawning and changes in endogenous estradiol levels in the zebra mussel Dreissena polymorpha Aquat. Toxicol. 106-107 2012 123 130
O. Le Curieux-Belfond, S. Moslemi, M. Mathieu, and G.E. Sèralini Androgen metabolism in oyster Crassostrea gigas: evidence for 17ß-HSD activities and characterization of an aromatase-like activity inhibited by pharmacological compounds and a marine pollutant J. Steroid Biochem. Mol. Biol. 78 2001 359 366 (Pubitemid 33079111)
G.A. LeBlanc, M.P. Gooding, and R.M. Sternberg Testosterone-fatty acid esterification: a unique target for the endocrine toxicity of tributyltin to gastropods Integr. Comp. Biol. 45 2005 81 87 (Pubitemid 40748102)
W.K. Liu, Q. Li, and L. Kong Estradiol-17β and testosterone levels in the cockle Fulvia mutica during the annual reproductive cycle N. Z. J. Mar. Freshw. Res. 42 2008 417 424
A. Lyssimachou, J. Bachmann, and C. Porte Short-term exposure to the organotin compound triphenyltin modulates esterified steroid levels in females of Marisa cornuarietis Aquat. Toxicol. 89 2008 129 135
A. Lyssimachou, J.C. Navarro, J. Bachmann, and C. Porte Triphenyltin alters lipid homeostasis in females of the ramshorn snail Marisa cornuarietis Environ. Pollut. 157 2009 1714 1720
A. Lyssimachou, M. Ramon, and C. Porte Comparative study on the metabolism of the androgen precursor androstenedione in two gastropod species: in vitro alterations by TBT and TPT Comp. Biochem. Physiol. C 149 2009 409 413
P. Matthiessen, D. Arnold, A.C. Johnson, T.J. Pepper, T.G. Pottinger, and K.G.T. Pulman Contamination of headwater streams in the United Kingdom by oestrogenic hormones from livestock farms Sci. Total. Environ. 367 2006 616 630 (Pubitemid 44160494)
N. Nakada, H. Nyunoya, M. Nakamura, A. Hara, T. Iguchi, and H. Takada Identification of estrogenic compounds in wastewater effluent Environ. Toxicol. Chem. 23 2004 2807 2815 (Pubitemid 39603322)
T. Naokuni Induction of egg-laying by steroid hormones in slugs Comp. Biochem. Physiol. A 62 1979 273 278
A. Nieto, F. Borrull, E. Pocurull, and R.M. Marcé Occurrence of pharmaceuticals and hormones in sewage sludge Environ. Toxicol. Chem. 29 2010 1484 1489
J.-I. Nishikawa Imposex in marine gastropods may be caused by binding of organotins to retinoid X receptor Mar. Biol. 149 2006 117 124
E. Oberdörster, D. Rittschof, and P. McClellan-Green Testosterone metabolism in imposex and normal Ilyanassa obsoleta: comparison of field and TBTA Cl-induced imposex Mar. Pollut. Bull. 36 1998 144 151 (Pubitemid 28223285)
J. Oehlmann, U. Schulte-Oehlmann, M. Tillmann, and B. Markert Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part I: bisphenol A and octylphenol as xeno-estrogens Ecotoxicology 9 2000 383 397 (Pubitemid 32108386)
J. Oehlmann, U. Schulte-Oehlmann, J. Bachmann, M. Oetken, I. Lutz, W. Kloas, and T.A. Ternes Bisphenol A induces superfeminization in the ramshorn snail Marisa cornuarietis (Gastropoda: Prosobranchia) at environmentally relevant concentrations Environ. Health Perspect. 114 2006 127 133
E.F. Orlando, A.S. Kolok, G.A. Binzcik, J.L. Gates, M.K. Horton, C.S. Lambright, L.E. Gray Jr., A.M. Soto, and L.J. Guillette Jr. Endocrine-disrupting effects of cattle feedlot effluent on an aquatic sentinel species, the fathead minnow Environ. Health Perspect. 112 2004 353 358 (Pubitemid 38351399)
M. Ortiz-Zarragoitia, and M.P. Cajaraville Intersex and oocyte atresia in a mussel population from the Biosphere's Reserve of Urdaibai (Bay of Biscay) Ecotoxicol. Environ. Saf. 73 2010 693 701
M.R. Peck, P. Labadie, C. Minier, and E.M. Hill Profiles of environmental and endogenous estrogens in the zebra mussel Dreissena polymorpha Chemosphere 69 2007 1 8 (Pubitemid 47187492)
C. Porte, G. Janer, L.C. Lorusso, M. Ortiz-Zarragoitia, M.P. Cajaraville, M.C. Fossi, and L. Canesi Endocrine disruptors in marine organisms: approaches and perspectives Comp. Biochem. Physiol. C 143 2006 303 315 (Pubitemid 44183641)
A.M. Reitzel, and A.M. Tarrant Correlated evolution of androgen receptor and aromatase revisited Mol. Biol. Evol. 27 2010 2211 2215
C. Riva, C. Porte, A. Binelli, and A. Provini Evaluation of 4-nonylphenol in vivo exposure in Dreissena polymorpha: bioaccumulation, steroid levels and oxidative stress Comp. Biochem. Physiol. C 152 2010 175 181
M.J.J. Ronis, and A.Z. Mason The metabolism of testosterone by the periwinkle (Littorina littorea) in vitro and in vivo: effects of tributyltin Mar. Environ. Res. 42 1996 161 166 (Pubitemid 26188768)
L. Salste, P. Leskinen, M. Virta, and L. Kronberg Determination of estrogens and estrogenic activity in wastewater effluent by chemical analysis and the bioluminescent yeast assay Sci. Total. Environ. 378 2007 343 351 (Pubitemid 46654155)
M.M. Santos, C.C. ten Hallers-Tjabbes, N. Vieira, J.P. Boon, and C. Porte Cytochrome P450 differences in normal and imposex-affected female whelk Buccinum undatum from the open North Sea Mar. Environ. Res. 54 2002 661 665 (Pubitemid 35286491)
M.M. Santos, L.F.C. Castro, M.N. Vieira, J. Micael, R. Morabito, P. Massanisso, and M.A. Reis-Henriques New insights into the mechanism of imposex induction in the dogwhelk Nucella lapillus Comp. Biochem. Physiol. C 141 2005 101 109 (Pubitemid 40961588)
M.M. Santos, M.A. Reis-Henriques, R. Guillot, D. Lima, R. Franco-Duarte, I. Mendes, S. QueirÛs, and L.F.C. Castro Anti-androgenic effects of sewage treatment plant effluents in the prosobranch gastropod Nucella lapillus Comp. Biochem. Physiol. C 148 2008 87 93
U. Schulte-Oehlmann, M. Tillmann, B. Markert, and J. Oehlmann Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part II: Triphenyltin as a xeno-androgen Ecotoxicology 9 2000 399 412 (Pubitemid 32108387)
U. Schulte-Oehlmann, M. Oetken, J. Bachmann, and J. Oehlmann Effects of Ethinyloestradiol and Methyltestosterone in Prosobranch Snails K. Kümmerer, 2004 Springer Berlin Heidelberg Berlin, Germany
A.P. Scott Do mollusks use vertebrate sex steroids as reproductive hormones? Part I: critical appraisal of the evidence for the presence, biosynthesis and uptake of steroids Steroids 77 2012 1450 1468
N.W. Shappell Estrogenic activity in the environment: municipal wastewater effluent, river, ponds, and wetlands J. Environ. Qual. 35 2006 122 132 (Pubitemid 43185181)
A. Siah, J. Pellerin, A. Benosman, J.P. Gagné, and J.C. Amiard Seasonal gonad progesterone pattern in the soft-shell clam Mya arenaria Comp. Biochem. Physiol. A 132 2002 499 511 (Pubitemid 34521882)
A.M. Soto, C. Sonnenschein, K.L. Chung, M.F. Fernandez, N. Olea, and F.O. Serrano The E-SCREEN assay as a tool to identify estrogens: an update on estrogenic environmental pollutants Environ. Health Perspect. 103 Suppl. 7 1995 113 122
N. Spooner, P.E. Gibbs, G.W. Bryan, and L.J. Goad The effect of tributyltin upon steroid titres in the female dogwhelk, Nucella lapillus, and the development of imposex Mar. Environ. Res. 32 1991 37 49
R.M. Sternberg, and G.A. LeBlanc Kinetic characterization of the inhibition of acyl coenzyme A: steroid acyltransferases by tributyltin in the eastern mud snail (Ilyanassa obsoleta) Aquat. Toxicol. 78 2006 233 242 (Pubitemid 43783207)
R.M. Sternberg, A.K. Hotchkiss, and G.A. LeBlanc The contribution of steroidal androgens and estrogens to reproductive maturation of the eastern mud snail Ilyanasa obsoleta Gen. Comp. Endocrinol. 156 2008 15 26
R.M. Sternberg, A.K. Hotchkiss, and G.A. Leblanc Synchronized expression of retinoid X receptor mRNA with reproductive tract recrudescence in an imposex-susceptible mollusc Environ. Sci. Technol. 42 2008 1345 1351 (Pubitemid 351287202)
R.M. Sternberg, M.P. Gooding, A.K. Hotchkiss, and G.A. LeBlanc Environmental-endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin-induced imposex in prosobranchs Ecotoxicology 19 2010 4 23
O.F. Tankoua, C. Amiard-Triquet, F. Denis, C. Minier, C. Mouneyrac, and B. Berthet Physiological status and intersex in the endobenthic bivalve Scrobicularia plana from thirteen estuaries in northwest France Environ. Pollut. 167 2012 70 77
Y. Tashiro, A. Takemura, H. Fujii, K. Takahira, and Y. Nakanishi Livestock wastes as a source of estrogens and their effects on wildlife of Manko tidal flat, Okinawa Mar. Pollut. Bull. 47 2003 143 147 (Pubitemid 36627634)
J.W. Thornton, E. Need, and D. Crews Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling Science 301 2003 1714 1717 (Pubitemid 37174363)
K.L. Thorpe, M. Gross-Sorokin, I. Johnson, G. Brighty, and C.R. Tyler An assessment of the model of concentration addition for predicting the estrogenic activity of chemical mixtures in wastewater treatment works effluents Environ. Health Perspect. 114 2006 90 97
M. Tillmann, U. Schulte-Oehlmann, M. Duft, B. Markert, and J. Oehlmann Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part III: Cyproterone acetate and vinclozolin as antiandrogens Ecotoxicology 10 2001 373 388 (Pubitemid 33070882)
D.J. van der Horst, and P.A. Voogt Biosynthesis and composition of sterols and sterol esters in the land snail Cepaea nemoralis (L.) (Gastropoda, Pulmonata, Stylommatophora) Comp. Biochem. Physiol. B 42 1972 1 6
C. Wang, and R.P. Croll Effects of sex steroids on in vitro gamete release in the sea scallop, Placopecten magellanicus Invertebr. Reprod. Dev. 44 2003 89 100 (Pubitemid 37546142)
C. Wang, and R.P. Croll Effects of sex steroids on gonadal development and gender determination in the sea scallop, Placopecten magellanicus Aquaculture 238 2004 483 498 (Pubitemid 39123663)
C. Wang, and R.P. Croll Effects of sex steroids on spawning in the sea scallop, Placopecten magellanicus Aquaculture 256 2006 423 432 (Pubitemid 43767180)
C.G. Wang, Z.Y. Huang, Y.X. Chen, Y. Zhao, and Z.H. Zuo Effect of tributyltin at environmentally relevant doses on levels of sex hormones in female clams Meretrix meretrix Bull. Environ. Contam. Toxicol. 75 2005 1163 1167 (Pubitemid 43086933)