Imposex in Nucella lapillus, a bioindicator for TBT contamination: re-survey along the Portuguese coast to monitor the effectiveness of EU regulation
Introduction
Tributyltin (TBT) has been used extensively since the late 1960s as a biocide in antifouling paints for ships' hulls. This organometallic compound is very efficient in preventing settlement of organisms on ships' hulls, but has deleterious effects in non-target organisms (Fent, 1996). Gastropods and bivalves are among the most sensitive organisms to the toxic effects of organotins. In the intertidal dogwhelk Nucella lapillus, TBT in concentrations above 0.5 ng Sn dm−3 induces the development of male sexual characteristics in females (Gibbs and Bryan, 1986), a penis and a vas deferens, a phenomenon called imposex (Smith, 1971). In advanced stages of imposex, the growth of a vas deferens may result in occlusion of the oviduct, thus causing sterility (Gibbs and Bryan, 1986). Due to their sensitive response, several snail species have been used world wide as bioindicators of TBT contamination Gibbs et al., 1987, Ten Hallers-Tjabbes et al., 1994, Stroben et al., 1995, Oehlmann et al., 1996, Swennen et al., 1997, Solé et al., 1998, Santos et al., 2000.
Based on the deleterious effects of organotins in non-target organisms, several countries have regulated the use of organotins on ships smaller than 25 m (Ten Hallers-Tjabbes, 1997), including Portugal in 1993 (D.L. 54/93). In 1989 the European Union published a Directive (89/677/CEE) banning TBT from vessels smaller than 25 m; in 1990 the Marine Environment Protection Committee (MEPC) of the International Maritime Organization (IMO) adopted a resolution recommending to ban TBT from such small vessels (Resolution MEPC 46(30)) (Anon., 1990). Although a maximum leaching rate of 4 μg TBT cm−2 d−1 was recommended for ships larger than 25 m, no further restrictions on the use of organotins as biocides in antifouling paints were considered, on the assumption that concentrations of TBT in the open sea were too low to cause effects. More recently, TBT was also shown to have a similar impact in the open sea, the imposex incidence being correlated with shipping density (Ten Hallers-Tjabbes et al., 1994, Ten Hallers-Tjabbes et al., 2002, Swennen et al., 1997, Anonymous, 2001a; Gomez Ariza et al., submitted).
Along the Iberian coast, several studies have shown that imposex and organotin contamination is widespread in estuarine and coastal areas Gibbs et al., 1997, Pessoa and Oliveira, 1997, Barroso et al., 2000, Santos et al., 2000 and in offshore waters (Anon., 2001a; Santos et al., submitted; Gomez-Ariza et al., submitted). The intertidal area along the Portuguese coast was extensively surveyed in 1995–1996, using imposex in the dogwhelk N. lapillus to asses gradients of TBT contamination at 27 sites, over a distance of 600 km of coastline (Santos et al., 2000).
The present study aimed to investigate the effectiveness of the legislation that banned the use of organotins for ships smaller than 25 m. The frequency and degree of imposex in N. lapillus were examined at the same sites as our previous survey of 1995–1996.
Section snippets
Material and methods
A total of 25 sites were re-visited between October 2000 and July 2001, five years after the initial survey (Fig. 1). The sampling sites included the major commercial harbours, as well as some important fishing harbours, marinas and other sites with minor shipping activity.
Fifty individuals, if possible, were collected at each site during spring tides, and transported live to the laboratory. Individuals larger than 26 mm and those showing eroded shells were not collected, since they would
Results
During the present survey, females showing imposex were found at all sampling sites (Table 1). At 14 sites, imposex frequency in females was higher in 2000–2001 than in 1995–1996, at three sites imposex frequency was lower, and no change had occurred at eight sites. A similar pattern was found for VDSI and RPSI values. Both indexes increased at 13 sites, decreased at five sites, and remained unchanged at six sites. Both the increase in imposex frequency and VDSI were statistically significant
Discussion
The results of this study show that the restrictions introduced in Portugal in 1993 banning the use of organotins on ships under 25 m have not been effective in reducing imposex in dogwhelk populations. This indicates that since the first survey TBT contamination along the Portuguese coast has not declined in most of the surveyed areas.
In both surveys, sites in northern and central Portugal had the higher levels of imposex, which is in agreement with the concentration of shipping activities in
Acknowledgements
We would like to thank Emı́lia Castro and Paula Enes for their help during the sampling. We would also like to acknowledge the comments of two anonymous referees which helped us to improve the manuscript. M. M. Santos was funded by a grant Praxis XXI BD/ 13739/97 from the Portuguese Foundation for Science and Technology.
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