Reproductive impacts of tributyltin (TBT) and triphenyltin (TPT) in the hermaphroditic freshwater gastropod Lymnaea stagnalis

Environmental Toxicology and Chemistry

Volumn 32, Issue 7, 2013, Pages 1552-1560

  Giusti, Arnaud ^a,b   Barsi, Alpar ^b   Dugué, Maël ^b   Collinet, Marc ^b   Thomé, Jean Pierre ^a   Joaquim Justo, Célia ^a   Roig, Benoit ^c,d   Lagadic, Laurent ^b   Ducrot, Virginie ^b  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b Ecology and Ecosystem Health   (France)

^c EHESP SCHOOL OF PUBLIC HEALTH   (France)

^d UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Endocrine disruptors; Mollusk toxicology; Organotin; Reproductive toxicity; Toxicity mechanisms

Indexed keywords

ENDOCRINE DISRUPTOR; MOLLUSK TOXICOLOGY; ORGANOTINS; REPRODUCTIVE TOXICITIES; TOXICITY MECHANISMS;

ANIMALS; MOLLUSCS; ORGANOMETALLICS; WATER;

TOXICITY;

TRIBUTYLTIN; TRIPHENYLTIN;

EGG DEVELOPMENT; ENDOCRINE DISRUPTOR; FRESHWATER ECOSYSTEM; GASTROPOD; GROWTH RATE; REPRODUCTION; REPRODUCTIVE STRATEGY; SURVIVAL; TOXICITY TEST;

ARTICLE; CONTROLLED STUDY; EGG LAYING; FERTILITY; GROWTH; HABITAT; LYMNAEA STAGNALIS; NONHUMAN; PRIORITY JOURNAL; REPRODUCTION; SURVIVAL;

ANIMALS; ENDOCRINE DISRUPTORS; FRESH WATER; LYMNAEA; ORGANOTIN COMPOUNDS; REPRODUCTION; RISK ASSESSMENT; TRIALKYLTIN COMPOUNDS; WATER POLLUTANTS, CHEMICAL;

BASOMMATOPHORA; GASTROPODA; LYMNAEA STAGNALIS; MOLLUSCA;

EID: 84878703010     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1002/etc.2200     Document Type: Article

References (66)

1. Hobler C, Andrade AJM, Grande SW, Gericke C, Talsness CE, Appel KE, Chahoud I, Grote K. 2010. Sex-dependent aromatase activity in rat offspring after pre- and postnatal exposure to triphenyltin chloride. Toxicology 276:198-205.
2. International Maritime Organization. 2005. International Convention on the Control of Harmful Anti-fouling Systems on Ships adopted on the 05/10/2001. IMO [cited 15 October 2012]. Available from: http://www.imo.org. London, UK
3. International Programme on Chemical Safety. 1990. Tributyltin compounds. Environmental Health Criteria 116. World Health Organisation, Geneva, Switzerland.
4. De Oliveira CR, Dos Santos D, Dos Santos Madureira LA, De Marchi MRR. 2010. Speciation of butyltin derivatives in surface sediments of three southern Brazilian harbors. J Hazard Mater 181:851-856.
5. Bigatti G, Primost MA, Cledón M, Averbuj A, Theobald N, Gerwinski W, Arntz W, Morriconi E, Penchaszadeh PE. 2009. Biomonitoring of TBT contamination and imposex incidence along 4700km of Argentinean shoreline (SW Atlantic: From 38S to 54S). Mar Pollut Bull 58:695-701.
6. Antizar-Ladislao B. 2008. Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment. A review. Environ Int 34:292-308.
7. Forsyth DS, Casey V. 2003. Butyltin compounds in retail mollusc products. Food Add Contam 20:445-452.
8. Duft M, Schulte-Oehlmann U, Tillmann M, Markert B, Oehlmann J. 2003. Toxicity of triphenyltin and tributyltin to the freshwater mud snail Potamopyrgus antipodarum in a new sediment biotest. Environ Toxicol Chem 22:145-152.
9. Strand J, Jacobsen JA. 2005. Accumulation and trophic transfer of organotins in a marine food web from the Danish coastal waters. Sci Total Environ 350:72-85.
10. Harino H, Fukushima M, Kawai S. 2000. Accumulation of butyltin and phenyltin compounds in various fish species. Arch Environ Contam Toxicol 39:13-19.
11. Alzieu C. 1998. Tributyltin: Case study of a chronic contaminent in the coastal environment. Ocean Coast Manag 40:23-36.
12. Gibbs PE, Pascoe PL, Burt GR. 1988. Sex change in the female dog-whelk, Nucella lapillus, induced by tributyltin from antifouling paints. J Mar Biol Assoc UK 68:715-731.
13. Horiguchi T, Lee J-H, Park J-C, Cho H-S, Shiraishi H, Morita M. 2012. Specific accumulation of organotin compounds in tissues of the rock shell, Thais clavigera. Mar Environ Res 76:56-62.
14. Bauer B, Fioroni P, Schulte-Oehlmann U, Oehlmann J, Kalbfus W. 1997. The use of Littorina littorea for tributyltin (TBT) effect monitoring-Results from the German TBT survey 1994/1995 and laboratory experiments. Environ Pollut 96:299-309.
15. Lyssimachou A, Navarro JC, Bachmann J, Porte C. 2009. Triphenyltin alters lipid homeostasis in females of the ramshorn snail Marisa cornuarietis. Environ Pollut 157:1714-1720.
16. Schulte-Oehlmann U, Tillmann M, Markert B, Oehlmann J. 2000. Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part II: Triphenyltin as a xeno-androgen. Ecotoxicology 9:399-412.
17. Horiguchi T, Shiraishi H, Shimizu M, Morita M. 1997. Effects of triphenyltin chloride and five other organotin compounds on the development of imposex in the rock shell, Thais clavigera. Environ Pollut 95:85-91.
18. Leung KMY, Morley NJ, Grist EPM, Morritt D, Crane M. 2004. Chronic toxicity of tributyltin on development and reproduction of the hermaphroditic snail Physa fontinalis: Influence of population density. Mar Environ Res 58:157-162.
19. Leung KMY, Grist EPM, Morley NJ, Morritt D, Crane M. 2007. Chronic toxicity of tributyltin to development and reproduction of the European freshwater snail Lymnaea stagnalis (L.). Chemosphere 66:1358-1366.
20. Lagadic L, Coutellec M-A, Caquet T. 2007. Endocrine disruption in aquatic pulmonate molluscs: Few evidences, many challenges. Ecotoxicology 16:45-59.
21. Czech P, Weber K, Dietrich DR. 2001. Effects of endocrine modulating substances on reproduction in the hermaphroditic snail Lymnaea stagnalis L. Aquat Toxicol 53:103-114.
22. Schulte-Oehlmann U, Bettin C, Fioroni P, Oehlmann J, Stroben E. 1995. Marisa cornuarietis (Gastropoda, prosobranchia): A potential TBT bioindicator for freshwater environments. Ecotoxicology 4:372-384.
23. Janer G, Lyssimachou A, Bachmann J, Oehlmann J, Schulte-Oehlmann U, Porte C. 2006. Sexual dimorphism in esterified steroid levels in the gastropod Marisa cornuarietis: The effect of xenoandrogenic compounds. Steroids 71:435-444.
24. Segner H, Caroll K, Fenske M, Janssen CR, Maack G, Pascoe D, Schäfers 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 54:302-314.
25. Ceulemans M, Slaets S, Adams F. 1998. Speciation of organotin in environmental sediment samples. Talanta 46:395-405.
26. Jadhav S, Bhosale D, Bhosle N. 2011. Baseline of organotin pollution in fishes, clams, shrimps, squids and crabs collected from the west coast of India. Mar Pollut Bull 62:2213-2219.
27. Horiguchi T, Shiraishi H, Shimizu M, Morita M. 1994. Imposex and organotin compounds in Thais clavigera and T. bronni in Japan. J Mar Biol Assoc UK 74:651-669.
28. Lyssimachou A, Ramon M, Porte C. 2009. 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 149:409-413.
29. Jarne P, David P, Pointier J, Koene J. 2010. Basommatophoran gastropods. In Córdoba-Aguilar A, Leonard JL, eds, The Evolution of Primary Sexual Characters in Animals. Oxford University Press Oxford, UK, pp. 173-196.
30. Coutellec M-A, Lagadic L. 2006. Effects of self-fertilization, environmental stress and exposure to xenobiotics on fitness-related traits of the freshwater snail Lymnaea stagnalis. Ecotoxicology 15:199-213.
31. Matthiessen P. 2008. An assessment of endocrine disruption in mollusks and the potential for developing internationally standardized mollusk life cycle test guidelines. Integr Environ Assess Manag 4:274-284.
32. Koene J. 2010. Neuro-endocrine control of reproduction in hermaphroditic freshwater snails: Mechanisms and evolution. Front Behav Neurosci 4:167-167.
33. Organization for Economic Cooperation and Development. 1999. Report from the OECD consultation on testing in Fish, 28-29 October, London, UK. Paris, France.
34. Geraerts WPM. 1976. The control of ovulation in the hermaphroditic freshwater snail Lymnaea stagnalis by the neurohormone of the caudodorsal cells. Gen Comp Endocrinol 28:350-357.
35. Ducrot V, Teixeira-Alves M, Lopes C, Delignette-Muller M-L, Charles S, Lagadic L. 2010. Development of partial life-cycle experiments to assess the effects of endocrine disruptors on the freshwater gastropod Lymnaea stagnalis: A case-study with vinclozolin. Ecotoxicology 19:1312-1321.
36. Organization for Economic Cooperation and Development. 2000. Guidance document on aquatic toxicity testing of difficult substances and mixtures. OECD Series on Testing and Assessment 23. ENV/JM/MONO (2000) 6. Paris, France.
37. 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 188:205-223.
38. Giusti A, Ducrot V, Joaquim-Justo C, Laurent L, Thomé J-P. 2010. Effects of androgenic and anti-androgenic substances on the freshwater gastropod Lymnaea stagnalis. Abstracts, SETAC Europe 20th Annual Meeting: Science and Technology for Environmental Protection, Seville, Spain, 23-27 May, 2010, p 146.
39. Barsi A, Ducrot V, Jager T, Lagadic L. 2011. Mechanistic modelling of effects of endocrine disruptors in populations of the pond snail Lymnaea stagnalis. Krakow.
40. Zimmer E, Jager T, Ducrot V, Lagadic L, Kooijman SALM. 2012. Juvenile food limitation in standardized tests: A warning to ecotoxicologists. Ecotoxicology 21:2195-2204.
41. Bluzat R, Jonot O, Lespinasse G, Seuge J. 1979. Chronic toxicity of acetone in the fresh water snail Lymnea stagnalis. Toxicology 14:179-190.
42. Lanzer. 1999. Toxicity of nonylphenol during embryo growth in Lymnaea stagnalis GSF report. L. Institut für Ökologische Chemie, Neuherberg, Munich, Germany.
43. Bandow C, Weltje L. 2012. Development of an embryo toxicity test with the pond snail Lymnaea stagnalis using the model substance tributyltin and common solvents. Sci Total Environ 435-436:90-95.
44. British Standards Institution. 2004. Water Quality: Determination of Selected Organotin Compounds-Gas Chromatographic Method. London, UK, p 31.
45. Belgers JDM, Aalderink GH, Arts GHP, Brock TCM. 2011. Can time-weighted average concentrations be used to assess the risks of metsulfuron-methyl to Myriophyllum spicatum under different time-variable exposure regimes? Chemosphere 85:1017-1025.
46. Organization for Economic Cooperation and Development. 2006. Current Approaches in the Statistical Analysis of Ecotoxicity Data: A Guidance to Application. Paris, France.
47. Duggleby RG. 1981. A nonlinear regression program for small computers. Anal Biochem 110:9-18.
48. Vindimian E. 2001. The biological monitoring of toxic impacts on the environment. Cell Mol Biol 47:1309-1318.
49. Alzieu C, Héral M, Thibaud Y, Dardignac M-J, Feuillet M. 1982. Influence des peintures antisalissures à base d'organostatiques sur la calcification de l'huitre Crassostrea gigas. Rev Trav Inst Peches Mar 45:101-116.
50. Nesci S, Ventrella V, Trombetti F, Pirini M, Borgatti AR, Pagliarani A. 2011. Tributyltin (TBT) and dibutyltin (DBT) differently inhibit the mitochondrial Mg-ATPase activity in mussel digestive gland. Toxicol In Vitro 25:117-124.
51. Gooding MP, Wilson VS, Folmar LC, Marcovich DT, LeBlanc GA. 2003. The biocide tributyltin reduces the accumulation of testosterone as fatty acid esters in the mud snail (Ilyanassa obsoleta). Environ Health Perspect 111:426-430.
52. Castro LFC, Lima D, Machado A, Melo C, Hiromori Y, Nishikawa J, Nakanishi T, Reis-Henriques MA, Santos MM. 2007. Imposex induction is mediated through the retinoid X receptor signalling pathway in the neogastropod Nucella lapillus. Aquat Toxicol 85:57-66.
53. Spooner N, Gibbs PE, Bryan GW, Goad LJ. 1991. The effect of tributyltin upon steroid titres in the female dogwhelk, Nucella lapillus, and the development of imposex. Mar Environ Res 32:37-49.
54. Santos MM, Castro LFC, Vieira MN, Micael J, Morabito R, Massanisso P, Reis-Henriques MA. 2005. New insights into the mechanism of imposex induction in the dogwhelk Nucella lapillus. Comp Biochem Physiol C 141:101-109.
55. Bettin C, Oehlmann J, Stroben E. 1996. TBT-induced imposex in marine neogastropods is mediated by an increasing androgen level. Helgol Meeresunters 50:299-317.
56. Sternberg RM, LeBlanc GA. 2006. Kinetic characterization of the inhibition of acyl coenzyme A: Steroid acyltransferases by tributyltin in the eastern mud snail (Ilyanassa obsoleta). Aquat Toxicol 78:233-242.
57. Ronis MJJ, Mason AZ. 1996. The metabolism of testosterone by the periwinkle (Littorina littorea) in vitro and in vivo: Effects of tributyl tin. Mar Environ Res 42:161-166.
58. LeBlanc GA, Gooding MP, Sternberg RM. 2005. Testosterone-fatty acid esterification: A unique target for the endocrine toxicity of tributyltin to gastropods. Integr Comp Biol 45:81-87.
59. Sternberg RM, Gooding MP, Hotchkiss AK, LeBlanc GA. 2010. Environmental-endocrine control of reproductive maturation in gastropods: Implications for the mechanism of tributyltin-induced imposex in prosobranchs. Ecotoxicology 19:4-23.
60. Kanayama T, Kobayashi N, Mamiya S, Nakanishi T, Nishikawa J-I. 2005. Organotin compounds promote adipocyte differentiation as agonists of the peroxisome proliferator-activated receptor γ/retinoid X receptor pathway. Mol Pharmacol 67:766-774.
61. Nishikawa J-I. 2006. Imposex in marine gastropods may be caused by binding of organotins to retinoid X receptor. Mar Biol 149:117-124.
62. Nakanishi T. 2008. Endocrine disruption induced by organotin compounds; organotins function as a powerful agonist for nuclear receptors rather than an aromatase inhibitor. J Toxicol Sci 33:269-276.
63. Nishikawa J-I, Mamiya S, Kanayama T, Nishikawa T, Shiraishi F, Horiguchi T. 2004. Involvement of the retinoid X receptor in the development of imposex caused by organotins in gastropods. Environ Sci Technol 38:6271-6276.
64. Morcillo Y, Porte C. 1997. Interaction of tributyl- and triphenyltin with the microsomal monooxygenase system of molluscs and fish from the Western Mediterranean. Aquat Toxicol 38:35-46.
65. Schulte-Oehlmann U. 1997. Fortpflanzungsstörungen bei Süßund Brackwasserschnecken-Einfluß der Umweltchemikalie Tributylzinn. Wissenschaft und Technik Verlag, Berlin, Germany.
66. Ketata I, Denier X, Hamza-Chaffai A, Minier C. 2008. Endocrine-related reproductive effects in molluscs. Comp Biochem Physiol C 147:261-270.