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Organotins and Imposex in Europe: A Pre-ban and Post-ban Perspective

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Book cover Biological Effects by Organotins

Abstract

The use of tributyltin (TBT) and, to a lesser extent, triphenyltin (TPT) as biocides in antifouling paint formulations during the last decades of the twentieth century was responsible for the global contamination of the coastal and offshore areas of the European aquatic environment. This widespread contamination was responsible for extensive deleterious effects in nontarget organisms particularly in gastropods, which, as a consequence of TBT exposure, developed imposex in a dose-dependent manner. Over the last decades, more than 20 gastropod species registering the occurrence of imposex were used by European researchers to ascertain the degree of TBT pollution in the European coastal and marine environment. In this chapter, we will evaluate the status of organotin (OT) contamination in European countries, using imposex in gastropods as a surrogate. The temporal trends uncovered are evaluated under the light of the 2003 European ban (Directive 2002/62/EC and Regulation 782/2003) and the AFS Convention (entered into force in 2008). The reduction of TBT pollution is addressed under the same light. Overall, we conclude that significant reductions in imposex levels started to emerge after the European ban (2003), though those reductions were more pronounced from 2008 onward. The most recent surveys disclose that the recovery of the ecosystems from the “TBT nightmare” is ongoing.

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Notes

  1. 1.

    PARCOM: PARIS COMMISSION. The commission was a group of experts who advised North Sea countries on environmental policy and legislation. The Paris Convention of 1974 was unified with the Oslo Convention from 1972, updated, and extended by the OSPAR Convention in 1992 (www.ospar.org).

  2. 2.

    RPSI (relative penis size index) = FPL(female penis length)3× 100/MPL(male penis length)3) is used for N. lapillus, whereas for N. reticulatus the RPLI (relative penis length index) is used (RPLI = FPL × 100/MPL), due to the penis size and shape.

Abbreviations

AF:

Antifouling

AFS Convention:

International Convention on the Control of Harmful Antifouling Systems on Ships

EAC:

Environmental Assessment Criterion

EC:

European Commission

EcoQO:

Ecological Quality Objective

IMO:

International Maritime Organization

OSPAR:

Convention for the Protection of the Marine Environment of the North-East Atlantic

OTs:

Organotin compounds

PARCOM:

Paris Commission

PVC:

Polyvinyl chloride

REACH:

Registration, Evaluation, Authorization and Restriction of Chemicals (European Union Regulation)

RPLI:

Relative penis length index

RPSI:

Relative penis size index

TBT:

Tributyltin

TPT:

Triphenyltin

VDSI:

Vas deferens sequence index

References

  • Alzieu C (1998) Tributyltin: case study of a chronic contaminant in the coastal environment. Ocean Coast Manage 40:23–26. doi:10.1016/S0964-5691(98)00036-2

    Article  Google Scholar 

  • Alzieu C (2000a) Environmental impact of TBT: the French experience. Sci Total Environ 258(1–2):99–102. doi:10.1016/S0048-9697(00)00510-6

    Article  CAS  Google Scholar 

  • Alzieu C (2000b) Impact of tributyltin on marine invertebrates. Ecotoxicology 9(1–2):71–76. doi:10.1023/A:1008968229409

    Article  CAS  Google Scholar 

  • Axiak V, Vella AJ, Micallef D, Chircop P, Mintoff B (1995) Imposex in hexaplex trunculus (Gastropoda: Muricidae): first results from biomonitoring of tributyltin contamination in the mediterranean. Mar Biol 121(4):685–691. doi:10.1007/bf00349304

    Article  Google Scholar 

  • Axiak V, Vella AJ, Agius D, Bonnici P, Cassar G, Casson R, Chircop P, Micallef D, Mintoff B, Sammut M et al (2000) Evaluation of environmental levels and biological impact of TBT in Malta (central Mediterranean). Sci Total Environ 258(1–2):89–97

    Article  CAS  Google Scholar 

  • Axiak V, Micallef D, Muscat J, Vella A, Mintoff B (2003) Imposex as a biomonitoring tool for marine pollution by tributyltin: some further observations. Environ Int 28(8):743–749

    Article  CAS  Google Scholar 

  • Axiak V, Galea S, Guillaumier R, Herrera P, Micallef D, Muscat J, VeIia N (2012) Imposex as surveillance biomonitoring tool of pollution by the antifouling agent, TBT after its ban: Malta, a case study. Fresen Environ Bull 21(10):3035–3041

    CAS  Google Scholar 

  • Bailey SK, Davies IM (1988) Tributyltin contamination in the Firth of Forth (1975–1987). Sci Total Environ 76(2):185–192. doi:http://dx.doi.org/10.1016/0048-9697(88)90106-4

  • Bailey SK, Davies IM (1989) The effects of tributyltin on dogwhelks (Nucella lapillus) from Scottish coastal waters. J Mar Biol Assoc UK 69(2):335–354. doi:10.1017/S0025315400029453

    Article  CAS  Google Scholar 

  • Barreiro R, Quintela M, Ruiz JM (1999) Aphally and imposex in Nucella lapillus from Galicia (NW Spain): incidence, geographical distribution and consequences for the biomonitoring of TBT contamination. Mar Ecol Prog Ser 185:229–238. doi:10.3354/meps185229

    Article  CAS  Google Scholar 

  • Barreiro R, González R, Quintela M, Ruiz JM (2001) Imposex, organotin bioaccumulation and sterility of female Nassarius reticulatus in polluted areas of NW Spain. Mar Ecol Prog Ser 218:203–212. doi:10.3354/meps218203

    Article  CAS  Google Scholar 

  • Barroso CM, Moreira MH (2002) Spatial and temporal changes of TBT pollution along the Portuguese coast: inefficacy of the EEC directive 89/677. Mar Pollut Bull 44(6):480–486. doi:10.1016/S0025-326X(01)00260-0

    Article  CAS  Google Scholar 

  • Barroso CM, Moreira MH, Gibbs PE (2000) Comparison of imposex and intersex development in four prosobranch species for TBT monitoring of a southern European estuarine system (Ria de Aveiro, NW Portugal). Mar Ecol Prog Ser 201:221–232. doi:10.3354/meps201221

    Article  Google Scholar 

  • Barroso CM, Moreira MH, Bebianno MJ (2002) Imposex, female sterility and organotin contamination of the prosobranch Nassarius reticulatus from the Portuguese coast. Mar Ecol Prog Ser 230:127–135. doi:10.3354/meps230127

    Article  Google Scholar 

  • Barroso CM, Reis-Henriques MA, Ferreira M, Gibbs PE, Moreira MH (2005) Organotin contamination, imposex and androgen/oestrogen ratios in natural populations of Nassarius reticulatus along a ship density gradient. Appl Organomet Chem 19(11):1141–1148. doi:10.1002/aoc.955

    Article  CAS  Google Scholar 

  • Barroso CM, Rato M, Verissimo A, Sousa A, Santos JA, Coelho S, Gaspar MB, Maia F, Galante-Oliveira S (2011) Combined use of Nassarius reticulatus imposex and statolith age determination for tracking temporal evolution of TBT pollution in the NW Portuguese continental shelf. J Environ Monit 13(11):3018–3025. doi:10.1039/C1EM10508F

    Article  CAS  Google Scholar 

  • 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(3):299–309. doi:http://dx.doi.org/10.1016/S0269-7491(97)00049-3

  • Birchenough AC, Barnes N, Evans SM, Hinz H, Kronke I, Moss C (2002a) A review and assessment of tributyltin contamination in the North Sea, based on surveys of butyltin tissue burdens and imposex/intersex in four species of neogastropods. Mar Pollut Bull 44(6):534–543

    Article  CAS  Google Scholar 

  • Birchenough AC, Evans SM, Moss C, Welch R (2002b) Re-colonisation and recovery of populations of dogwhelks Nucella lapillus (L.) on shores formerly subject to severe TBT contamination. Mar Pollut Bull 44(7):652–659

    Article  CAS  Google Scholar 

  • Blaber SJM (1970) The occurrence of a penis-like outgrowth behind the right tentacle in spent females of Nucella lapillus (L.). Proc Malacol Soc Lond 39:231–233

    Google Scholar 

  • Bray S, McVean EC, Nelson A, Herbert RJH, Hawkins SJ, Hudson MD (2012) The regional recovery of Nucella lapillus populations from marine pollution, facilitated by man-made structures. J Mar Biol Assoc UK 92(7):1585–1594

    Article  Google Scholar 

  • Bryan GW, Gibbs PE, Hummerstone LG, Burt GR (1986) The decline of the gastropod Nucella lapillus around the south-West England: evidence for the effect of tributyltin from antifouling paints. J Mar Biol Assoc UK 66:611–640. doi:10.1017/S0025315400042247

    Article  CAS  Google Scholar 

  • Bryan GW, Gibbs PE, Burt GR, Hummerstone LG (1987) The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-term field and laboratory experiments. J Mar Biol Assoc UK 67(3):525–544. doi:10.1017/S0025315400027272

    Article  CAS  Google Scholar 

  • Bryan GW, Burt GR, Gibbs PE, Pascoe PL (1993) Nassarius reticulatus (Nassariidae: Gastropoda) as an indicator of tributyltin pollution before and after TBT restrictions. J Mar Biol Assoc UK 73:913–929. doi:10.1017/S0025315400034809

    Article  CAS  Google Scholar 

  • Burton ED, Phillips IR, Hawker DW (2004) Sorption and desorption behavior of tributyltin with natural sediments. Environ Sci Technol 38(24):6694–6700

    Article  CAS  Google Scholar 

  • Cacciatore F, Noventa S, Antonini C, Formalewicz M, Gion C, Berto D, Gabellini M, Brusà RB (2016) Imposex in Nassarius nitidus (Jeffreys, 1867) as a possible investigative tool to monitor butyltin contamination according to the Water Framework Directive: A case study in the Venice Lagoon (Italy). Ecotox Environ Safe. doi:http://dx.doi.org/10.1016/j.ecoenv.2015.12.039

  • Chiavarini S, Massanisso P, Nicolai P, Morabito R (2003) Butyltins concentration levels and imposex occurrence in snails from the Sicilian coasts (Italy). Chemosphere 50:311–319

    Article  CAS  Google Scholar 

  • Couceiro L, Díaz J, Albaina N, Barreiro R, Irabien JA, Ruiz JM (2009) Imposex and gender-independent butyltin accumulation in the gastropod Nassarius reticulatus from the Cantabrian coast (N Atlantic Spain). Chemosphere 76(3):424–427. doi:10.1016/j.chemosphere.2009.03.035

    Article  CAS  Google Scholar 

  • Cuevas N, García Alonso JI, Larreta J, Rodríguez JG, Sariego C, Zorita I (2014) Monitoring the effectiveness of the European tributyltin regulation on the Basque coast (northern Spain) by assessing imposex in two gastropod species (Nassarius reticulatus and Nassarius nitidus). Chemistry and Ecology:1–7. doi:10.1080/02757540.2014.894991

    Google Scholar 

  • Davies IM, Bailey SK (1991) The impact of tributyltin from large vessels on the dogwhelk Nucella lapillus (L.) populations around scottish oil ports. Mar Environ Res 32:202–211. doi:10.1016/0141-1136(91)90042-7

    Article  Google Scholar 

  • de Wolf H, de Coen W, Backeljan T, Blust R (2001) Intersex and sterility in the periwinkle Littorina littorea (Mollusca: Gastropoda) along the Western Scheldt estuary, the Netherlands. Mar Environ Res 52:249–255

    Article  Google Scholar 

  • Evans SM, Leksono T, McKinnel PD (1995) Tributyltin pollution: a diminishing problem following legislation limiting the use of TBT-based antifouling paints. Mar Pollut Bull 30(1):14–21. doi:10.1016/0025-326X(94)00181-8

    Article  CAS  Google Scholar 

  • Evans SM, Evans PM, Leksono T (1996) Widespread recovery of dogwhelks, Nucella lapillus (L.), from tributyltin contamination in the North Sea and Clyde Sea. Mar Pollut Bull 32(3):263–269. doi:10.1016/0025-326X(95)00127-9

    Article  CAS  Google Scholar 

  • Evans SM, Birchenough AC, Fletcher H (2000a) The value and validity of community-based research: TBT contamination of the North Sea. Mar Pollut Bull 40(3):220–225

    Article  CAS  Google Scholar 

  • Evans SM, Kerrigan E, Palmer N (2000b) Causes of imposex in the dogwhelk Nucella lapillus (L.) and its use as a biological indicator of tributyltin contamination. Mar Pollut Bull 40(3):212–219

    Article  CAS  Google Scholar 

  • EVISA (2009) European Virtual Institute for Speciation Analysis – EU bans certain organotin compounds. http://www.speciation.net/News/EU-bans-certain-organotin-compounds-;~/2009/06/05/4298.html

  • Galante-Oliveira S, Langston WJ, Burt GR, Pereira ME, Barroso CM (2006) Imposex and organotin body burden in the dog-whelk Nucella lapillus L. along the Portuguese coast. Appl Organomet Chem 20:1–4

    Article  CAS  Google Scholar 

  • Galante-Oliveira S, Oliveira I, Jonkers N, Langston WJ, Pacheco M, Barroso CM (2009) Imposex levels and tributyltin pollution in Ria de Aveiro (NW Portugal) between 1997 and 2007: evaluation of legislation effectiveness. J Environ Monit 11(7):1405–1411. doi:10.1039/B900723G

    Article  CAS  Google Scholar 

  • Galante-Oliveira S, Oliveira I, Pacheco M, Barroso CM (2010a) Hydrobia ulvae imposex levels at Ria de Aveiro (NW Portugal) between 1998 and 2007: a counter-current bioindicator? J Environ Monit 12(2):500–507

    Article  CAS  Google Scholar 

  • Galante-Oliveira S, Oliveira I, Santos JA, Pereira ML, Pacheco M, Barroso CM (2010b) Factors affecting RPSI in imposex monitoring studies using Nucella lapillus (L.) as bioindicator. J Environ Monit 12:1055

    Article  CAS  Google Scholar 

  • Galante-Oliveira S, Oliveira I, Ferreira N, Santos JA, Pacheco M, Barroso C (2011) Nucella lapillus L. imposex levels after legislation prohibiting TBT antifoulants: temporal trends from 2003 to 2008 along the Portuguese coast. J Environ Monit 13(2):304–312

    Article  CAS  Google Scholar 

  • Garaventa F, Pellizzato F, Faimali M, Terlizzi A, Medakovic D, Geraci S, Pavoni B (2006) Imposex in Hexaplex trunculus at some sites on the North mediterranean coast as a base-line for future evaluation of the effectiveness of the total ban on organotin based antifouling paints. In: Martens K, Queiroga H, Cunha MR et al (eds) Marine biodiversity: patterns and processes, assessment, threats, management and conservation. Springer Netherlands, Dordrecht, pp 281–287. doi:10.1007/1-4020-4697-9_24

    Chapter  Google Scholar 

  • Garaventa F, Centanni E, Pellizzato F, Faimali M, Terlizzi A, Pavoni B (2007) Imposex and accumulation of organotin compounds in populations of Hexaplex trunculus (Gastropoda, Muricidae) from the Lagoon of Venice (Italy) and Istrian Coast (Croatia). Mar Pollut Bull 54(5):615–622

    Article  CAS  Google Scholar 

  • Gibbs PE (1993) A male genital defect in the dog-whelk, Nucella lapillus (Neogastropoda), favouring survival in a TBT-polluted area. J Mar Biol Assoc UK 73(03):667–678. doi:10.1017/S0025315400033208

    Article  Google Scholar 

  • Gibbs PE (1999) Biological effects of contaminants: use of imposex in the dogwhelk (Nucella lapillus) as a bioindicator of tributyltin pollution. International Council for the exploration of the Sea, Copenhagen

    Google Scholar 

  • Gibbs PE (2009) Long-term tributyltin (TBT)-induced sterilization of neogastropods: persistence of effects in Ocenebra erinacea over 20 years in the vicinity of Falmouth (Cornwall, UK). J Mar Biol Assoc UK 89(01):135–138. doi:10.1017/S0025315408002336

    Article  CAS  Google Scholar 

  • Gibbs PE, Bryan GW, Pascoe PL, Burt GR (1987) The use of the dog-whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. J Mar Biol Assoc UK 67(3):507–523. doi:10.1017/S0025315400027260

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gibbs PE, Bebianno MJ, Coelho MR (1997) Evidence of the differential sensitivity of neogastropods to tributyltin (TBT) pollution, with notes on a species (Columbella rustica) lacking the imposex response. Environ Technol 18(12):1219–1224. doi:10.1080/09593331808616643

    Article  CAS  Google Scholar 

  • Gil R, Avital G, Stewart ME, Yehuda B (2000) Unregulated use of TBT-based antifouling paints in Israel (eastern Mediterranean): high contamination and imposex levels in two species of marine gastropods. Mar Ecol Prog Ser 192:229–238

    Article  Google Scholar 

  • Giltrap M, Macken A, Davoren M, Minchin D, McGovern E, Foley B, Strand J, McHugh B (2009) Use of caged Nucella lapillus and Crassostrea gigas to monitor tributyltin-induced bioeffects in Irish coastal waters. Environ Toxicol Chem 28(8):1671–1678

    Article  CAS  Google Scholar 

  • Goldberg ED (1986) TBT: An environmental dilemma. Environment 28:17–44. doi:10.1080/00139157.1986.9928814

    Article  Google Scholar 

  • Goméz-Ariza JL, Santos MM, Morales E, Giráldez I, Sánchez-Rodas D, Vieira N, Kemp JF, Boon JP, ten Hallers-Tjabbes CC (2006) Organotin contamination in the Atlantic Ocean off the Iberian Peninsula in relation to shipping. Chemosphere 64(7):1100–1108. doi:10.1016/j.chemosphere.2005.11.068

    Article  CAS  Google Scholar 

  • Guðmundsdóttir LÓ, Ho KKY, Lam JCW, Svavarsson J, Leung KMY (2011) Long-term temporal trends (1992–2008) of imposex status associated with organotin contamination in the dogwhelk Nucella lapillus along the Icelandic coast. Mar Pollut Bull 63(5–12):500–507. doi:http://dx.doi.org/10.1016/j.marpolbul.2011.02.012

  • Hallers-Tjabbes CCT, Kemp JF, Boon JP (1994) Imposex in whelks (Buccinum undatum) from the open North Sea: Relation to shipping traffic intensities. Mar Pollut Bull 28(5):311–313. doi:http://dx.doi.org/10.1016/0025-326X(94)90156-2

  • Harding MJ, Davies IM (2000) A field evaluation of international monitoring guidelines for the biological effects of tributyltin. J Environ Monit 2(5):404–409

    Article  CAS  Google Scholar 

  • Harding MJC, Rodger GK, Davies IM, Moore JJ (1997) Partial recovery of the dogwhelk (Nucella lapillus) in Sullom Voe, Shetland from tributyltin contamination. Mar Environ Res 44(3):285–304. doi:10.1016/S0141-1136(97)00008-1

    Article  CAS  Google Scholar 

  • Harding MJC, Davies IM, Bailey SK, Rodger GK (1999) Survey of imposex in dogwhelks (Nucella lapillus) from north sea coasts. Appl Organomet Chem 13(7):521–538

    Article  CAS  Google Scholar 

  • Hoch M (2001) Organotin compounds in the environment – an overview. Appl Geochem 16(7–8):719–743. doi:10.1016/S0883-2927(00)00067-6

    Article  CAS  Google Scholar 

  • Huet M, Fioroni P, Oehlmann J, Stroben E (1995) Comparison of imposex response in three prosobranch species. Hydrobiologia 309:29–35. doi:10.1007/BF00014469

    Article  Google Scholar 

  • Huet M, Paulet YM, Glémarec M (1996a) Tributyltin (TBT) pollution in the coastal waters of West Brittany as indicated by imposex in Nucella lapillus. Mar Environ Res 41(2):157–167

    Article  CAS  Google Scholar 

  • Huet M, Paulet YM, Pennec M (1996b) Survival of Nucella lapillus in a tributyltin-polluted area in west Brittany: a further example of a male genital defect (Dumpton syndrome) favouring survival. Mar Biol 125(3):543–549

    Article  Google Scholar 

  • Huet M, Paulet YM, Clavier J (2004) Imposex in Nucella lapillus: a ten year survey in NW Brittany. Mar Ecol Prog Ser 270:153–161

    Article  Google Scholar 

  • Huet M, le Goïc N, Gibbs P (2008) Appearance of a genetically-based pollution resistance in a marine gastropod, Nucella lapillus, in south-west Brittany: a new case of Dumpton syndrome. J Mar Biol Assoc UK 88(7):1475–1479. doi:10.1017/S0025315408002038

    Article  Google Scholar 

  • IMO (1999) Anti-fouling systems moving towards the non-toxic solution. International Maritime Organization, London. http://www.imo.org/includes/blastDataOnly.asp/data_id%3D7986/FOULING2003.pdf

  • Jakob S, Jens AJ (2002) Imposex in two sublittoral neogastropods from the Kattegat and Skagerrak: the common whelk Buccinum undatum and the red whelk Neptunea antiqua. Mar Ecol Prog Ser 244:171–177

    Article  Google Scholar 

  • Jörundsdóttir K, Svavarsson J, Leung KMY (2005) Imposex levels in the dogwhelk Nucella lapillus (L.) – Continuing improvement at high latitudes. Mar Pollut Bull 51:744–749. doi:10.1016/j.marpolbul.2005.04.012

    Article  CAS  Google Scholar 

  • Laranjeiro FM, Sousa ACA, Takahashi S, Tanabe S, Barroso CM (2010) Combination of field monitoring and laboratory bioassays for the assessment of TBT pollution in Ria de Aveiro. In: Hamamura N, Suzuki S, Mendo S, Barroso CM, Iwata H, Tanabe S (eds) Interdisciplinary Studies on Environmental Chemistry – Biological Responses to Contaminants: from molecular to community level., Aveiro, Portugal, 2010. Interdisciplinary Studies on Environmental Chemistry TERRAPUB, Tokyo, pp 175–188

    Google Scholar 

  • Laranjeiro F, Pérez S, Navarro P, Carrero JA, Beiras R (2015a) The usefulness of a sediment bioassay with the gastropod Nassarius reticulatus in tributyltin monitoring programs. Chemosphere 139:550–557. doi:http://dx.doi.org/10.1016/j.chemosphere.2015.07.076

  • Laranjeiro F, Sánchez-Marín P, Galante-Oliveira S, Barroso C (2015b) Tributyltin pollution biomonitoring under the Water Framework Directive: Proposal of a multi-species tool to assess the ecological quality status of EU water bodies. Ecol Indic 57 (0):525–535. doi:http://dx.doi.org/10.1016/j.ecolind.2015.04.039

  • Maran C, Centanni E, Pellizzato F, Pavoni B (2006) Organochlorine compounds (polychlorinated biphenyls and pesticides) and polycyclic aromatic hydrocarbons in populations of Hexaplex trunculus affected by imposex in the lagoon of Venice, Italy. Environ Toxicol Chem 25(2):486–495

    Article  CAS  Google Scholar 

  • Miller KL, Fernandes TF, Read PA (1999) The recovery of populations of dogwhelks suffering from imposex in the Firth of Forth 1987-1997/98. Environ Pollut 106(2):183–192. doi:10.1016/S0269-7491(99)00076-7

    Article  CAS  Google Scholar 

  • Minchin A, Minchin D (1997) Dispersal of TBT from a Fishing Port Determined Using the Dogwhelk Nucella Lapillus as an Indicator. Environ Technol 18(12):1225–1234. doi:10.1080/09593331808616644

    Article  CAS  Google Scholar 

  • Minchin D, Oehlmann J, Duggan CB, Stroben E, Keatinge M (1995) Marine TBT antifouling contamination in Ireland, following legislation in 1987. Mar Pollut Bull 30(10):633–639. doi:10.1016/0025-326X(95)00016-G

    Article  CAS  Google Scholar 

  • Minchin D, Stroben E, Oehlmann J, Bauer B, Duggan CB, Keatinge M (1996) Biological indicators used to map organotin contamination in Cork Harbour, Ireland. Mar Pollut Bull 32(2):188–195. doi:10.1016/0025-326X(95)00120-C

    Article  CAS  Google Scholar 

  • Minchin D, Bauer B, Oehlmann J, Schulte-Oehlmann U, Duggan CB (1997) Biological indicators used to map organotin contamination from a fishing port, Killybegs, Ireland. Mar Pollut Bull 34(4):235–243

    Article  CAS  Google Scholar 

  • Morgan E, Murphy J, Lyons R (1998) Imposex in Nucella lapillus from TBT contamination in South and South-West Wales: a continuing problem around ports. Mar Pollut Bull 36(10):840–843. doi:10.1016/S0025-326X(98)00087-3

    Article  CAS  Google Scholar 

  • Morton B (2009) Recovery from imposex by a population of the dogwhelk, Nucella lapillus (Gastropoda: Caenogastropoda), on the southeastern coast of England since May 2004: A 52-month study. Mar Pollut Bull 58(10):1530–1538

    Article  CAS  Google Scholar 

  • Nicolaus EM, Barry J (2015) Imposex in the dogwhelk (Nucella lapillus): 22-year monitoring around England and Wales. Environ Monit Assess 187(12):1–14

    Article  CAS  Google Scholar 

  • Oehlmann J, Bauer B, Minchin D, Schulte-Oehlmann U, Fioroni P, Markert B (1998) Imposex in Nucella lapillus and intersex in Littorina littorea: interspecific comparison of two TBT-induced effects and their geographical uniformity. Hydrobiologia 378(1–3):199–213

    Article  Google Scholar 

  • Oliveira IB, Richardson CA, Sousa AC, Takahashi S, Tanabe S, Barroso CM (2009) Spatial and temporal evolution of imposex in dogwhelk Nucella lapillus (L.) populations from North Wales, UK. J Environ Monit 11(8):1462–1468

    Article  CAS  Google Scholar 

  • Omae I (2006) Chemistry and fate of organotin antifouling biocides in the environment. In: Hutzinger O (ed) Handbook of Environmental Chemistry, Volume 5: Water Pollution, vol 5. Springer, Berlin/Heidelberg, pp 17–50. doi:10.1007/698-5-048

    Google Scholar 

  • OSPAR (2007) EcoQO Handbook: handbook for the application of ecological quality objectives in the North Sea. Biodiversity Series, 1st edn. OSPAR Commission

    Google Scholar 

  • OSPAR (2008) JAMP guidelines for contaminant-specific biological effects (OSPAR Agreement 2008-2009). OSPAR Convention For the Protection of the Marine Environment of the North-East Atlantic: Monitoring programs

    Google Scholar 

  • Pavoni B, Centanni E, Valcanover S, Fasolato M, Ceccato S, Tagliapietra D (2007) Imposex levels and concentrations of organotin compounds (TBT and its metabolites) in Nassarius nitidus from the Lagoon of Venice. Mar Pollut Bull 55(10–12):505–511

    Article  CAS  Google Scholar 

  • Pellizzato F, Centanni E, Marin MG, Moschino V, Pavoni B (2004) Concentrations of organotin compounds and imposex in the gastropod Hexaplex trunculus from the Lagoon of Venice. Sci Total Environ 332(1–3):89–100. doi:http://dx.doi.org/10.1016/j.scitotenv.2004.03.036

  • Peña J, Guerra M, Gaudencio MMK (1988) The occurrence of imposex in the gastropod Nucella lapillus at sites in Spain and Portugal. Lurralde 11:1–7

    Google Scholar 

  • Pessoa MF, Fernando A, Oliveira JS (2001) Use of imposex (Pseudohermaphroditism) as indicator of the occurrence of organotin compounds in Portuguese coastal waters – Sado and Mira estuaries. Environ Toxicol 16(3):234–241. doi:10.1002/tox.1029

    Article  CAS  Google Scholar 

  • Plejdrup JK, Simonsen V, Pertoldi C, Schøyen M, Bayley M (2006) Genetic and morphological diversity in populations of Nucella lapillus (L.; neogastropoda) in response to tributyltin contamination. Ecotox Environ Safe 64(2):146–154. doi:http://dx.doi.org/10.1016/j.ecoenv.2005.11.006

  • Poloczanska ES, Ansell AD (1999) Imposex in the whelks Buccinum undatum and Neptunea antiqua from the west coast of Scotland. Mar Environ Res 47(2):203–212. doi:http://dx.doi.org/10.1016/S0141-1136(98)00117-2

  • Power AJ, Keegan BF (2001) The significance of imposex levels and TBT contamination in the Red Whelk, Neptunea antiqua (L.) from the Offshore Irish Sea. Mar Pollut Bull 42(9):761–772. doi:http://dx.doi.org/10.1016/S0025-326X(00)00221-6

  • Prime M, Peharda M, Jelic K, Mladineo I, Richardson CA (2006) The occurrence of imposex in Hexaplex trunculus from the Croatian Adriatic. Mar Pollut Bull 52(7):810–812

    Article  CAS  Google Scholar 

  • Quintela M, Barreiro R, Ruiz JM (2000) The use of Nucella lapillus (L.) transplanted in cages to monitor tributyltin (TBT) pollution. Sci Total Environ 247(2–3):227–237

    Article  CAS  Google Scholar 

  • Quintela M, Barreiro R, Ruiz JM (2002) Dumpton syndrome reduces the tributyltin (TBT) sterilising effect on Nucella lapillus (L.) by limiting the development of the imposed vas deferens. Mar Environ Res 54(3–5):657–660

    Article  CAS  Google Scholar 

  • Quintela M, Couceiro L, Ruiz JM, Barreiro R (2006) Discovery of imposex in the gastropod Cyclope neritea now invading Galicia (north-west Spain). J Mar Biol Assoc UK 86(5):1171–1173. doi:10.1017/S0025315406014159

    Article  Google Scholar 

  • Ramon M, Amor MJ (2001) Increasing imposex in populations of Bolinus brandaris (Gastropoda: Muricidae) in the northwestern Mediterranean. Mar Environ Res 52(5):463–475

    Article  CAS  Google Scholar 

  • Ramón M, Amor MJ (2002) Reproductive cycle of Bolinus brandaris and penis and genital duct size variations in a population affected by imposex. J Mar Biol Assoc UK 82:435–442. doi:10.1017/s0025315402005696

    Article  Google Scholar 

  • Rank J (2009) Intersex in Littorina littorea and DNA damage in Mytilus edulis as indicators of harbour pollution. Ecotox Environ Safe 72(4):1271–1277. doi:http://dx.doi.org/10.1016/j.ecoenv.2008.12.008

  • Rato M, Sousa A, Quintã R, Langston W, Barroso C (2006) Assessment of inshore/offshore tributyltin pollution gradients in the Northwest Portugal continental shelf using Nassarius reticulatus as a bioindicator. Environ Toxicol Chem 25(12):3213–3220. doi:10.1897/06-167R.1

    Article  CAS  Google Scholar 

  • Rato M, Gaspar MB, Takahashi S, Yano S, Tanabe S, Barroso C (2008) Inshore/offshore gradients of imposex and organotin contamination in Nassarius reticulatus (L.) along the Portuguese coast. Mar Pollut Bull 56:1323–1331. doi:10.1016/j.marpolbul.2008.04.004

    Article  CAS  Google Scholar 

  • Rato M, Ferreira N, Santos J, Barroso CM (2009) Temporal evolution of imposex in Nassarius reticulatus (L.) along the Portuguese coast: the efficacy of EC regulation 782/2003. J Environ Monit 11:100–107. doi:10.1039/b810188d

    Article  CAS  Google Scholar 

  • Rodríguez JG, Borja Á, Franco J, García Alonso JI, Garmendia JM, Muxika I, Sariego C, Valencia V (2009a) Imposex and butyltin body burden in Nassarius nitidus (Jeffreys, 1867), in coastal waters within the Basque Country (northern Spain). Sci Total Environ 407(14):4333–4339. doi:http://dx.doi.org/10.1016/j.scitotenv.2009.04.002

  • Rodríguez JG, Tueros I, Borja Á, Franco J, Ignacio García Alonso J, Garmendia JM, Muxika I, Sariego C, Valencia V (2009b) Butyltin compounds, sterility and imposex assessment in Nassarius reticulatus (Linnaeus, 1758), prior to the 2008 European ban on TBT antifouling paints, within Basque ports and along coastal areas. Cont Shelf Res 29(8):1165–1173. doi:10.1016/j.csr.2009.01.005

  • Rodríguez JG, Rouget P, Franco J, Garmendia JM, Muxika I, Valencia V, Borja Á (2010) Evaluation of the use of transplanted Nassarius reticulatus (Linnaeus, 1758), in monitoring TBT pollution, within the European Water Framework Directive. Ecol Indic 10(4):891–895. doi:10.1016/j.ecolind.2009.12.005

    Article  CAS  Google Scholar 

  • Ruiz JM, Quintela M, Barreiro R (1998) Ubiquitous imposex and organotin bioaccumulation in gastropods Nucella lapillus from Galicia (NW Spain): a possible effect of nearshore shipping. Mar Ecol Prog Ser 164:237–244

    Article  CAS  Google Scholar 

  • Ruiz JM, Barreiro R, González JJ (2005) Biomonitoring organotin pollution with gastropods and mussels. Mar Ecol Prog Ser 287:169–176. doi:10.3354/meps287169

    Article  Google Scholar 

  • Ruiz JM, Barreiro R, Couceiro L, Quintela M (2008) Decreased TBT pollution and changing bioaccumulation pattern in gastropods imply butyltin desorption from sediments. Chemosphere 73(8):1253–1257. doi:10.1016/j.chemosphere.2008.07.029

    Article  CAS  Google Scholar 

  • Ruiz JM, Díaz J, Albaina N, Couceiro L, Irabien A, Barreiro R (2010) Decade-long monitoring reveals a transient distortion of baseline butyltin bioaccumulation pattern in gastropods. Mar Pollut Bull 60(6):931–934

    Article  CAS  Google Scholar 

  • Sánchez-Marín P, Oliveira IB, Sousa ACA, Takahashi S, Tanabe S, Galante-Oliveira S (2016) Evaluation of female aphally in imposex-affected populations of Nucella lapillus at the southernmost distributional limit of the species in Europe. J Mollus Stud 82(1):144–153. doi:10.1093/mollus/eyv043

    Google Scholar 

  • Santos MM, Vieira N, Santos AM (2000) Imposex in the Dogwhelk Nucella lapillus (L.) along the Portuguese Coast. Mar Pollut Bull 40(7):643–646

    Article  CAS  Google Scholar 

  • Santos MM, ten Hallers-Tjables CC, Santos AM, Vieira N (2002a) Imposex in Nucella lapillus, a bioindicator for TBT contamination: re-survey along the Portuguese coast to monitor the effectiveness of EU regulation. J Sea Res 48:217–223. doi:10.1016/S1385-1101(02)00166-1

    Article  CAS  Google Scholar 

  • Santos MM, ten Hallers-Tjables CC, Vieira N, Boon J, Porte C (2002b) Cytochrome P450 dfferences in normal and imposex-affected female whelk Buccinum undatum from the open North Sea. Mar Environ Res 54:661–665. doi:10.1016/S0141-1136(02)00150-2

    Article  CAS  Google Scholar 

  • Santos MM, Vieira N, Reis-Henriques MA, Santos AM, Gómez-Ariza JL, Giráldez I, ten Hallers-Tjabbes CC (2004) Imposex and butyltin contamination off the Oporto Coast (NW Portugal): a possible effect of the discharge of dredged material. Environ Int 30(6):793–798. doi:10.1016/j.envint.2004.01.005

    Article  CAS  Google Scholar 

  • Schulte-Oehlmann U, Oehlmann J, Fioroni P, Bauer B (1997) Imposex and reproductive failure in Hydrobia ulvae (Gastropoda: Prosobranchia). Mar Biol 128(2):257–266. doi:10.1007/s002270050090

    Article  Google Scholar 

  • Schulte-Oehlmann U, Oehlmann J, Bauer B, Fioroni P, Leffler US (1998) Toxico-kinetic and -dynamic aspects of TBT-induced imposex in Hydrobia ulvae compared with intersex in Littorina littorea (Gastropoda, Prosobranchia). Hydrobiologia 378(1–3):215–225

    Article  Google Scholar 

  • Shi HH, Huang CJ, Zhu SX, Yu XJ, Xie WY (2005) Generalized system of imposex and reproductive failure in female gastropods of coastal waters of mainland China. Mar Ecol Prog Ser 304:179–189. doi:10.3354/meps304179

    Article  Google Scholar 

  • Smith BS (1971) Sexuality in the american mud snail, Nassarius obsoletus Say. Proc Malacol Soc Lond 39:377–378

    Google Scholar 

  • Smith BS (1980) The estuarine mud snail, Nassarius obsoletus: abnormalities in the reproductive system. J Mollus Stud 46:247–256

    Google Scholar 

  • Smith BS (1981a) Male characteristics on female mud snails caused by antifouling bottom paints. J Appl Toxicol 1(1):22–25. doi:10.1002/jat.2550010106

    Article  CAS  Google Scholar 

  • Smith BS (1981b) Reproductive anomalies in stenoglossan snails related to pollution from marinas. J Appl Toxicol 1(1):15–21. doi:10.1002/jat.2550010105

    Article  CAS  Google Scholar 

  • Smith AJ, Thain JE, Barry J (2006) Exploring the use of caged Nucella lapillus to monitor changes to TBT hotspot areas: A trial in the River Tyne estuary (UK). Mar Environ Res 62(2):149–163

    Article  CAS  Google Scholar 

  • Solé M, Morcillo Y, Porte C (1998) Imposex in the commercial snail Bolinus brandaris in the northwestern Mediterranean. Environ Pollut 99(2):241–246. doi:http://dx.doi.org/10.1016/S0269-7491(97)00186-3

  • Son MH, Hughes RN (2000) Relationship between imposex and morphological variation of the shell in Nucella lapillus (Gastropoda: Thaididae). Estuar Coast Shelf Sci 50(5):599–606. doi:http://dx.doi.org/10.1006/ecss.2000.0592

  • Sousa A, Mendo S, Barroso CM (2005) Imposex and organotin contamination in Nassarius reticulatus (L) along the Portuguese coast. Appl Organomet Chem 19:315–323. doi:10.1002/aoc.856

    Article  CAS  Google Scholar 

  • Sousa A, Matsudaira C, Takahashi S, Tanabe S, Barroso C (2007) Integrative assessment of organotin contamination in a southern European estuarine system (Ria de Aveiro, NW Portugal): Tracking temporal trends in order to evaluate the effectiveness of the EU ban. Mar Pollut Bull 54(10):1645–1653. doi:10.1016/j.marpolbul.2007.07.005

    Article  CAS  Google Scholar 

  • Sousa A, Laranjeiro F, Takahashi S, Tanabe S, Barroso CM (2009) Imposex and organotin prevalence in a European post-legislative scenario: Temporal trends from 2003 to 2008. Chemosphere 77(4):566–573. doi:10.1016/j.chemosphere.2009.06.049

    Article  CAS  Google Scholar 

  • Sousa AA, Pastorinho MR, Takahashi S, Tanabe S (2013) Organotin Compounds from Snails to Humans. In: Lichtfouse E, Schwarzbauer J, Robert D (eds) Pollutant Diseases, Remediation and Recycling, vol 4, Environmental Chemistry for a Sustainable World. Springer International Publishing, Wien, pp 215–275. doi:10.1007/978-3-319-02387-8_4

    Chapter  Google Scholar 

  • Sousa ACA, Pastorinho MR, Takahashi S, Tanabe S (2014) History on organotin compounds, from snails to humans. Environ Chem Lett 12(1):117–137. doi:10.1007/s10311-013-0449-8

    Article  CAS  Google Scholar 

  • Spence SK, Hawkins SJ, Santos RS (1990) The Mollusc Thais haemastoma -An Exhibitor of ‘Imposex’ and Potential Biological Indicator of Tributyltin Pollution. Mar Ecol 11(2):147–156. doi:10.1111/j.1439-0485.1990.tb00235.x

    Article  CAS  Google Scholar 

  • Stagličić N, Prime M, Žoko M, Erak Z, Brajčić D, Blaževic D, Madiraza K, Jelić K, Peharda M (2008) Imposex incidence in Hexaplex trunculus from Kaštela Bay, Adriatic Sea. Acta Adriat 49(2):159–164

    Google Scholar 

  • Stroben E, Oehlmann J, Fioroni P (1992) The morphological expression of imposex in Hinia reticulata (Gastropoda: Buccinidae): a potential indicator of tributyltin pollution. Mar Biol 113:625–636. doi:10.1007/BF00349706

    Article  Google Scholar 

  • Svavarsson J (2000) Imposex in the Dogwhelk (Nucella lapillus) due to TBT Contamination: Improvement at High Latitudes. Mar Pollut Bull 40(11):893–897

    Article  CAS  Google Scholar 

  • Svavarsson J, Granmo A, Ekelund R, Szpunar J (2001) Occurence and effects of organotins on adult common whelk (Buccinum undatum) (Mollusca, Gastropoda) in harbours and in a simulated dreadging site. Mar Pollut Bull 42(5):370–376

    Article  CAS  Google Scholar 

  • Ten Hallers-Tjabbes CC, Kemp JF, Boon JP (1994) Imposex in whelks (Buccinum undatum) from the open North Sea: Relation to shipping traffic intensities. Mar Pollut Bull 28(5):311–313. doi:10.1016/0025-326X(94)90156-2

    Article  Google Scholar 

  • ten Hallers-Tjables CC, Wegener JW, van Hattum BAGM, Kemp JF, ten Hallers E, Reitsema T, Boon J (2003) Imposex and organotin concentrations in Buccinum undatum and Neptunea antiqua from the North Sea: relationship to shipping density and hydrographical conditions. Mar Environ Res 55:203–233

    Article  Google Scholar 

  • Terlizzi A, Geraci S, Minganti V (1998) Tributyltin (TBT) pollution in the coastal waters of Italy as indicated by imposex in Hexaplex trunculus (Gastropoda, Muricidae). Mar Pollut Bull 36(9):749–752. doi:http://dx.doi.org/10.1016/S0025-326X(98)00027-7

  • Terlizzi A, Geraci S, Gibbs PE (1999) Tributyltin (TBT)‐induced imposex in the Neogastropod Hexaplex trunculus in Italian coastal waters: Morphological aspects and ecological implications. Ital J Zool 66(2):141–146. doi:10.1080/11250009909356248

    Article  CAS  Google Scholar 

  • Terlizzi A, Delos AL, Garaventa F, Faimali M, Geraci S (2004) Limited effectiveness of marine protected areas: imposex in Hexaplex trunculus (Gastropoda, Muricidae) populations from Italian marine reserves. Mar Pollut Bull 48(1–2):188–192. doi:http://dx.doi.org/10.1016/j.marpolbul.2003.10.019

  • Van den Broeck H, De Wolf H, Backeljau T, Blust R (2009) Comparative assessment of reproductive impairment in the gastropod mollusc Littorina littorea along the Belgian North Sea coast. Sci Total Environ 407(8):3063–3069. doi:http://dx.doi.org/10.1016/j.scitotenv.2008.12.050

  • Vasconcelos P, Gaspar MB, Castro M (2006) Imposex in Hexaplex (Trunculariopsis) trunculus (Gastropoda: Muricidae) from the Ria Formosa lagoon (Algarve coast – Southern Portugal). Mar Pollut Bull 52(3):337–341

    Google Scholar 

  • Vasconcelos P, Gaspar MB, Barroso CM (2010a) Imposex in Bolinus brandaris from the Ria formosa lagoon (southern Portugal): usefulness of “single-site baselines” for environmental monitoring. J Environ Monit 12(10):1823–1832

    Article  CAS  Google Scholar 

  • Vasconcelos P, Moura P, Barroso CM, Gaspar MB (2010b) Size matters: importance of penis length variation on reproduction studies and imposex monitoring in Bolinus brandaris (Gastropoda: Muricidae). Hydrobiologia:1–13

    Google Scholar 

  • WHO (1990) Environmental health criteria for tributyltin compounds. In: Environmental health criteria, vol 116. World Health Organization, Geneva

    Google Scholar 

  • Wilson JG, Minchin D, McHugh B, McGovern E, Tanner CJ, Giltrap M (2015) Declines in TBT contamination in Irish coastal waters 1987–2011, using the dogwhelk (Nucella lapillus) as a biological indicator. Mar Pollut Bull 100(1):289–296. doi:http://dx.doi.org/10.1016/j.marpolbul.2015.08.038

  • Wirzinger G, Vogt C, Bachmann J, Hasenbank M, Liers C, Stark C, Ziebart S, Oehlmann J (2007) Imposex of the netted whelk Nassarius reticulatus (Prosobranchia) in Brittany along a transect from a point source. Cah Biol Mar 48(1):85–94

    Google Scholar 

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Sousa, A.C.A., Pastorinho, M.R. (2017). Organotins and Imposex in Europe: A Pre-ban and Post-ban Perspective. In: Horiguchi, T. (eds) Biological Effects by Organotins. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56451-5_5

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