Tributyltin pollution: A diminishing problem following legislation limiting the use of TBT-based anti-fouling paints

M a r i n e Pollution Bulletin

~

Pergamon

0025-326X(94)00181-2

Marine Pollution Bulletin, Vol. 30, No. 1, pp. 14-21, 1995 Elsevier Science Ltd Printed in Great Britain 0025-326X/95 $9.50+0.00

Tributyltin Pollution: A Diminishing Problem Following Legislation Limiting the Use of TBT-Based Anti-fouling Paints S. M. EVANS, T. LEKSONO and P. D. McKINNELL Department of Marine Sciences & Coastal Management, University of Newcastle upon Tyne, NE1 7RU, UK

There is substantial evidence that tributyitin (TBT) contamination has decreased following the introduction of legislation prohibiting the use of TBT-based paints on vessels less than 25 m in length. Ambient levels of TBT have decreased in the water column, sediments and tissues of molluscs, and there has been recovery of dogwhelks and oysters from imposex and shell deformation, respectively. Severe pollution is now restricted primarily to hotspots of boating activity, such as ports. There is no evidence that it is a major problem in open seas and oceanic waters. There are now indications that imposex is less specific than has been supposed. While the response will still be useful in monitoring recovery of populations of Nucella lapillus from the effects of TBT pollution, its general use as a bioindicator of TBT is questionable.

Tributyltin (TBT) achieved notoriety during the early 1980s as a result of its use as an active biocide in antifouling paints. It was used either as a substitute for organomercury, arsenic or lead boosters in copperbased paints or as the sole biocidal agent. It was described as the most toxic substance ever deliberately introduced into the aquatic environment (Goldberg, 1986), and caused damage by leaching from the coatings applied to boat hulls and aquaculture cages into the water column. Particularly high concentrations of it occurred, therefore, in the vicinities of fish farms and areas of high boat use (Davies et al., 1987; Clark et al., 1988). TBT is almost universally toxic and has been used as a fungicide, bactericide, insecticide and wood preservative. It is known to be harmful to a range of aquatic biota, including microalgae (Beaumont & Newman, 1986), molluscs and crustaceans (Rexrode, 1987; Langston et al., 1990), fish (Wester et al., 1990) and 14

invertebrate communities of seagrass beds (Kelly et al., 1990a,b). The best documented cases of its impact on non-target marine organisms were however those on the Pacific oyster Crassostrea gigas (Thunberg) and the dogwhelk Nucella lapillus (L.). The first evidence of the harmful effects of TBT on oysters came from Arcachon Bay on the west coast of France in the mid-1970s. Oyster culture and pleasure boating are traditional activities there, and TBT contamination from boats was linked to high mortalities of oyster larvae and such severe malformations of the shells of adults that they were unmarketable (Alzieu et al., 1981-1982; Claisse & Alzieu, 1993). Female dogwhelks develop the condition known as imposex in response to TBT poisoning. Male characters, including a penis and vas deferens, become superimposed on the females' genitalia. In extreme cases, the vas deferens occludes the opening of the pallial oviduct, preventing the release of egg capsules and rendering the female effectively sterile. Bryan et al. (1986) provided a convincing case that it was responsible for the decline of populations of N. lapillus in south-west England in the 1980s. They showed that the severity of imposex correlated with tin tissue burdens (but not those of other metals) in dogwhelks, and that it could be induced either by exposing dogwhelks to leachates from anti-fouling paints or by transplanting them from 'clean' to TBT polluted sites.

Measuring TBT in the Marine Environment High concentrations of TBT and/or other organotoxins have been reported in coastal waters at several locations worldwide. They include France (Alzieu et al., 1986, 1989), the Mediterranean Sea (Gabriehdes et al., 1990), the Tyrrhenian Sea (Bacci & Gaggi, 1989), Bay of Naples (Cocchieri et al., 1993), Bahrain (Hasan & Juma, 1992), the UK (Cleary & Stebbing, 1987; Langston et al., 1987; Dowson et al., 1993), Canada

Volume 30/Number 1/January 1995

(Wolnickowski et aL, 1987), the USA (Makke et aL, 1989; Valkirs et al., 1991), New Zealand (King et aL, 1989) and Australia (Foale, 1993). There are, however, at least three difficulties in measuring TBT and in interpreting the results, especially in long-term monitoring programmes. First, TBT can be effective at concentrations which are close to the limits of detection (1-2 ng 1-1). Secondly, there are sometimes large spatial and temporal variations in concentrations of TBT at fixed locations because it may be released into the environment in pulses (e.g. from dry docks) which may be biologically harmful but missed by periodic sampling (Foale, 1993). Thirdly, TBT occurs at much higher levels in the surface microlayer and sediment than in the water column (Cleary, 1991). As a result of these difficulties bioassays have been developed as indicators of TBT contamination. They have been of three kinds. First, TBT accumulates in animal tissues, and measures of it in some molluscs have become standard in several monitoring programmes (e.g. Page & Widdows, 1991). Secondly, abnormal shell growth of oysters has been developed as a bioassay. Key et al. (1976) measured the cavity/depth ratio of shells, Alzieu et al. (1986) developed the shell thickness index and His & Robert (1987) measured shell density. Dyrynda (1992) found that, of these measures, shell thickness index was the most effective in revealing differences in oysters which had grown at TBT polluted or non-polluted sites. Thirdly, Gibbs et al. (1987) explored the use of imposex in N. lapillus as a bioindicator of TBT. They recommended two quantitative measures; (i) the relative penis size index (RPSI) which compares the size of the penis by the female with that of the male as a standard; and (ii) the vas deferens sequence index (VDSI), which recognises six stages primarily in the development of the vas deferens. Females at stages 1-4 of the vas deferens sequence (VDS) are capable of breeding but those at stages 5 and 6 are rendered sterile. Additional measures of the health and/or the reproductive status of populations of N. lapillus suffering from imposex have been made in some studies. They include assessments of abundance of dogwhelks on the shore, adult sex ratios (populations with male-biased ratios are likely to have suffered from high female mortality) and the proportions of juveniles in populations (as indicators of juvenile recruitment and therefore breeding performance) (Bryan et al., 1986; Evans etal., 1991; Douglas et al., 1993; Evans et al., 1994). Imposex has now been described in at least 72 species of gastropods, belonging to 49 genera (Oehlmann et al., 1991), and several whelks, other than N. lapillus, have been recommended as suitable bioindicators of TBT pollution. They include: Nucella lamellosa, N. cancaliculata and N. emarginata (Bright & Ellis, 1989; Alvarez & Ellis, 1990), Cronia margariticola, Drupella rugosa, Morula musiva and Thais luteostoma (Ellis & Pattisina, 1990), T. haemastoma (Spence et aL, 1990b), Lepsiella scobina and Lepsiella albomarginata (Smith & McVeagh, 1991; Stewart et al., 1992), T. orbita (Foale, 1993), T. orbita and M. marginata (Wilson et al., 1993)and L. vinosa (Nias et al., 1993).

The use of these bioassays suggested that there was worldwide TBT contamination (but see also below). Abnormalities in oyster shell growth were described, not only in France (see above), but in southern England (Wake et aL, 1991; Dyrynda, 1992), the USA (Stephenson et aL, 1986), Australia (Batley et aL, 1989) and New Zealand (King et aL, 1989). Similarly, imposex was described in N. lapillus in south-west England (Bryan et aL, 1086), north-east England (Evans et al., 1991; Douglas et aL, 1993), Scotland (Bailey & Davies, 1987; 1988a,b, 1989; Davies et aL, 1987; Evans et aL, 1994), the British coast including the Isle of Man (Spence et aL, 1990a), the Netherlands (Ritsema et aL, 1991) and the entire coastline of the North Sea (Harding et aL, 1992). In other whelk species, it occurred in Canada (Bright & Ellis, 1989; Alvarez & Ellis, 1990), Malaysia, Singapore and Indonesia (Ellis & Pattisina, 1990), Indonesia (Evans et aL, in press), West Africa (Spence et aL, 1990b), New Zealand (Smith & McVeagh, 1991; Stewart et aL, 1992) and Australia (Foale, 1993; Nias et aL, 1993; Wilson et aL, 1993). Not surprisingly, concerns about the impact of TBT on non-target organisms led to the introduction of legislative controls in a number of countries. France was the first to introduce them in response to the decline in oyster culture. Small, mainly pleasure, boats were believed to be the main source of contamination in coastal waters and France prohibited the use of TBTbased paints on vessels less than 25 m in length in 1982 (Alzieu, 1991). Similar regulations followed in the UK in 1987 (Waite et aL, 1991); USA in 1988 (Wade et aL, 1991); New Zealand in 1988 (Stewart et aL, 1992), Australia in 1989 (Foale, 1993; Wilson et aL, 1993) and Norway in 1989 (Harding et aL, 1992). There is an obvious need to assess the extent to which TBT contamination has declined since the introduction of these regulations. This is particularly important in view of conflicting evidence of recovery. Reports of reductions in TBT in French and British coastal waters, and of recovery of oyster farming in France (see, for example, Langston & Burt, 1991), do not accord with those of widespread sterility of dogwhelk populations in the North Sea (Harding et aL, 1992). The latter have been the basis of the claim in an ENDS report (Anon., 1993a) that the North Sea is currently so polluted that the survival of sensitive species such as the dogwhelk is endangered, and also the statement in the North Sea Quality Status Report (Anon., 1993b) that the reduction in the ability of the dogwhelk to reproduce is likely to have catastrophic effects on populations in the North Sea. There is an additional need to consider the earlier view expressed by Ellis & Pattisina (1990) that TBT pollution is global and that oyster and other mollusc resources are threatened everywhere in the world. These issues are considered in the present paper.

The Effectiveness of Regulations There is evidence of decreasing TBT pollution since the legislative ban on the use of TBT-based anti-fouling paints on boats less than 25 m in length: 15

Marine Pollution Bulletin

(1) There are several reports of declining levels of TBT in coastal waters. Alzieu et aL (1986) found that they were 5 to 10 times lower in the water column in 1985 than they had been in 1982 off the west coast of France; by 1989 they were generally lower than 5 ng 1-t (Michel & Alzieu, 1990). TBT concentrations have also declined since 1987 at coastal and estuarine sites in south-west England (Cleary, 1991), San Diego Bay, USA (Valkirs et al., 1991), south-east England (Dowson et al., 1993), north-west England (Douglas et aL, 1993), Puget Sound, Galveston Bay and Narragansett Bay, USA and Japan (Huggett et al., 1992; CEFIC, 1994). There are, nevertheless, concerns that some small boat owners may be flaunting the regulations. This would explain the continuing high concentrations of TBT in some marinas in France (Alzieu et al., 1989) and south-east England (Waite et al., 1991; Dowson et aL, 1993). TBT concentrations have decreased less rapidly in sediments than in the water column (Dowson et al., 1993) and Sarradin et aL (1991) have expressed concern about accumulation in them. Butyltins may have half-lives of several years in sediments and there are fears that TBT buried during earlier periods of high pollution may be remobilized through events such as storms or dredging operations. Sediment-bound TBT may also be available to deposit feeders (Langston & Burt, 1991). (2) Tin tissue burdens have declined in oysters Crassostrea virginica in the Gulf of Mexico between 1988 and 1990 (Wade et al., 1991), in mussels Mytilus edulis in San Diego Bay, USA from 1988 to 1990 (Valkirs et al., 1991), and in C. gigas and M. edulis in British waters between 1986 and 1992 (Waite et al., 1991; CEFIC, 1994). Similarly, tin concentrations decreased in N. lapillus at Loch Laxford, Scotland between 1986 and 1988 (Bailey & Davies, 1991), and Douglas et aL (1993) found that tissue concentrations in dogwhelks from northeast England in 1992 were at the low end of the range reported by Gibbs et al. (1987) from southwest England in the mid-1980s. (3) There have been substantial improvements in the health of oyster populations. Oyster farming has recovered in France, both in terms of spatfull and the production of marketable adults (Alzieu, 1991). Similarly, the oyster fishery in the River Blackwater in southern England, which had been closed since 1970, has reopened (Waite et al., 1991), and Dyrynda (1992) reported that TBT levels had declined sufficiently in much of Poole Harbour to allow a return to C. gigas mariculture. (4) Populations of dogwhelks have shown clear signs of recovery since the introduction of regulations. There are three lines of evidence: (i)

16

RPSIs have decreased since 1988 in British waters. The majority of sites sampled before that year had RPSI of more than 25 but, with the exception of Sullom Voe in 1990, each of those sampled after it had an index of less than

25 (Fig. 1). These data include studies of the north-east coast of England (Evans et al., 1991; Douglas et aL, 1993) and the Isle of Cumbrae, Scotland (Evans et aL, 1994) where particular sites have been resampled on several occasions. Declines in RPSI were statistically significant in these cases. There is also evidence of recovery from comparisons of the surveys made by Spence et aL (1990a) and Harding et aL (1992), of the south and east coast of Britain between 1986 and 1989, and 1992, respectively. Spence et al. (1990a) categorized populations of dogwhelks on the basis of RPSI (without publishing actual indexes). Many of their sites supported populations with RPSI of more than 40, and there were others at which there were either mature males only or at which dogwhelks were totally absent. Each of the sites sampled by Harding et aL (1992) had RPSI of < 40 (Fig. 2). Mean RPSI were also low along the north coast of France (17.6 + 4.1) and Sweden (18.4 + 8.2) in 1992 (Harding et al., 1992). (ii) Reproductive performances have improved since the introduction of regulations. Many populations of dogwhelks, which were sampled in the 1980s, were characterized by small numbers, or the total absence, of juveniles (Bryan et al., 1986; Evans et al., 1991, 1994; Douglas et al., 1993). They were evidently sterile, or nearly so. However, proportions of juveniles have been significantly higher at sites which have been resampled in north-east England (Douglas et aL, RPSI

~

22

60

I t,o

t

21

,13

I 1r

40

20

4

~28 t19

1985

1987

1989

1991

1993

Fig. 1 Mean RPSI (+ standard errors) from surveys of imposex in N. lapillus around the British coast. Data were from the following sources: 1, Torquay; 2, Faimouth; 3, Plymouth; 4, south-west England (Bryan et al., 1986); 5, Loch Sween; 6, Loch Crinan (Davies et al., 1987); 7-9, Loch Laxford (Bailey & Davies, 1991); 10-12, south-west England (Langston et al., 1990); 13, 14, north-east England (Evans et al., 1991); 15, north-east England (Douglas et al., 1993); 16, Sullom Voe, Shetland (Bailey & Davies, 1988b); 17, Sullom Voe (Harding et al., 1992); 18, Isle of Man (Spence et al., 1990a); 19, Loch Ewe; 20, Firth of Clyde; 21, Loch Spelve; 22, Loch Ardbhair (Bailey & Davies, 1989); 23, Firth of Forth (Bailey & Davies, 1988a); 2426, Isle of Cumbrae (Evans et al., 1994); 27, south and east coasts of Britain (Harding et al., 1992).

Volume 30/Number 1/January 1995

in three out of four studies for which data are available. They suggest that there is little impairment of breeding performance in populations which have RPSI of less than 25, which is higher than the mean score for all populations (except Sullom Voe) which has been sampled since 1987 (see Fig. 1). (iii) There have been significant increases in the abundance of dogwhelks on shores in northeast England (Douglas et al., 1993) and Isle of Cumbrae, Scotland (Evans et al., 1994) in recent surveys. This includes two cases in which dogwhelks have been recorded again on shores where they had been absent for several years.

E

Z~

Recovery is not however universal. Imp•sex scores were still high in several countries bordering the southern and eastern coasts of the North Sea (Harding et al., 1992). For example, RPSI in natural populations of N. lapillus in Norway (40.4+3.9), Denmark (33.5 + 10.8) and The Netherlands (44.3+ 5.6) were similar to those recorded in British waters in the 1980s. Mean VDSI were also high in these countries, ranging from 4.0+0.7 in Denmark to 4.3+0.1 in The Netherlands and 4.7 + 0.1 in Norway. Harding et al. (1992) used VDSI scores from sampling sites in order to infer the reproductive status of populations at them. These authors classified about one-third of sites along the entire North Sea coast as being totally sterile and a further third as having impaired breeding. The classifications are however misleading. There were almost certainly breeding females at many of the sites classed as sterile because the authors collected juveniles from

/ (a)

(b)

Fig. 2 Imposex in populations of N. lapillus at sites along the south and east coast of England when sampled: (a) by Spence et al. (1990a) between 1986 and 1989; and (b) by Harding et al. (1992) in 1991 The symbols are as follows: (3, RFSI less than 5; e, RPSI 5-40; O, either RPSI more than 40 or mature males only.

1993) and on the Isle of Cumbrae, Scotland (Evans et al., 1994) in the 1990s. Indeed, most populations of N. lapillus in Britain have probably been breeding at sustainable levels since 1987. Figure 3 shows that there were significantly negative correlations between RPSI and numbers of juveniles in populations

Juveniles a

Abundance C . - -"

Percent

C

100"

r S =-

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• rs

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- 0,7573

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rs=

- 0.1167 ns

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9

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75

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i 100

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Fig. 3 Relationships between proportions of juveniles in populations (as a measure of recent breeding performance) and imp•sex (RPSI) in four studies: (a) south-west England (Bryan et al., 1986); (b) north-east England (Evans et al., 1991); (c) Isle of Cumbrae, Scotland (Evans et al., 1994); and (d) north-east England (Douglas et al., 1993). Spearman rank coefficient of correlation (rs) are shown: ns, not significant; *p<0.05; ***p < 0.001. Bryan et al. (1986) scored abundance as: C, common; FC, fairly common; F, few; P, present; R, rare; A, absent.

17

Marine Pollution Bulletin

most of their sites for TBT tissue analyses. This included two of the three worst-affected sites, each along the Norwegian coast, with mean VDSI of more than 5. The authors found no females which they considered to be capable of reproducing at them. The case of Sullom Voe in the Shetland Islands is particularly interesting because it has been possible there to assess the environmental impact of TBT from large ships. Oil tankers visit the oil terminal but there are essentially no pleasure craft nor dry dock facilities in the Voe. Populations of N. lapillus are being slowly eliminated at the terminal itself and levels of imposex were high within the Voe in 1987 and 1990 (Davies & Bailey, 1991). These results suggest that TBT from large vessels is still a problem, although the finding by Harding et al. (1992) that dogwhelks, which were transplanted from a 'clean' site to Sullom Voe in 1992, developed no more than the mildest symptoms of imposex, is unexpected and unexplained.

A Local or Global Problem? The extent to which open seas and oceanic waters have been contaminated by TBT is unclear because sampling programmes have concentrated on centres of high boat use (or fish farms). Where programmes have included areas of open coast adjacent to such TBT hotspots the impact of TBT has been local. Imposexfree populations, or those with mild symptoms, have been described within a few kilometres of pollution at Loch Sween, Scotland (Davies et al., 1987), Sullom Voe, Shetland (Bailey & Davies, 1988b), Wellington Harbour and Porirua Inlet, New Zealand (Smith & McVeagh, 1991), Port Phillip Bay, Melbourne (Foale, 1993) and Ambon Bay, Indonesia (Evans et al., in press) (Fig. 4). There may have been some accumulation of TBT in semi-enclosed bodies of water, such as the Clyde Sea or the North Sea, because all populations of N. lapillus sampled in them have had measurable imposex, even those distant from areas of high boat use (e.g. Bailey & Davies, 1989; Evans et al., 1991; Harding et al., 1992; Douglas et al., 1993; Evans et al., 1994). The problem of TBT pollution was however localized, even in these seas, in the sense that there were diminishing gradients of imposex from TBT hotspots. Severe imposex was restricted mostly to ports and similar areas and, even within a few kilometres of them, there were populations of dogwhelks with low RPSIs and high proportions of juveniles (Fig. 5). It is also open to question whether these cases of mild imposex have been caused by agents other than TBT (see below). Offshore, imposex has been described in populations of whelks Buccinum undatum living close to busy commercial shipping lanes but is mild or absent in other areas (Hallers-Tjabbes et al., 1994). Incidence of imposex were low, symptoms occurring in less than 30% of females at all stations where more than 20 of them were sampled. Discussion There is substantial evidence that TBT contamination has declined in coastal areas of France and the UK 18

since the introduction of regulations prohibiting the use of TBT-based paints on boats less than 25 m in length and aquaculture cages. Ambient levels of TBT in the water column, sediments and mollusc tissues have decreased and their is evidence of recovery from abnormal shell growth in oysters and imposex in dogwhelks. While TBT contamination is a diminishing problem in most coastal areas, it is likely to persist in ports, such as Sullom Voe, which are frequented by large seagoing vessels. It should, however, become increasingly localized and restricted to them. Even now, severe pollution is confined primarily to such hotspots, and is virtually absent or mild on open coasts within distances of only a few kilometres of them. These data provide a different picture from those given in the North Sea Quality Status Report (Anon., 1993). They suggest that the regulations have been highly effective in reducing pollution from TBT-based paints. The extensive surveys of populations of N. lapillus in northern Europe, dating back to the mid-1980s, provide an excellent baseline against which recovery from imposex can be assessed. The standard measures of imposex, RPSI and VDSI, should however be used with caution. Although Gibbs et al. (1987) found that RPSI were reproducible over a 2 year period, the index may be subject to some variation because of (i) seasonal changes in the size of the male penis; or (ii) the presence of some populations of imposexed females which have developed a vas deferens but no penis (Oehlmann et al., 1991); or (iii) decrease in the size of the male penis due to malnutrition (Ritsema et al., 1991). There is also concern that there may be significant differences in the sizes of the male penis in populations of Lepsiella scobina no more than 500 m apart (Smith & McVeagh, 1991). VDSI is highly sensitive to low concentrations of TBT (Gibbs et al., 1987) but it has been measured in relatively few studies and, when it has been used to infer reproductive status by Harding et al. (1992), it appears to have been interpreted too pessimistically. Assessments of the proportions of juvenile dogwhelks in populations is a more direct measure of breeding performance because it reflects recruitment over the past 2 or 3 years (i.e. the time it takes for N. lapillus to mature; Feare, 1970). Healthy populations of dogwhelks normally have high proportions of juveniles in them (often in excess of 80%, for example, Evans et al. 1994) but severely imposexed ones may include few, if any, juveniles (e.g. Bryan etal., 1986; Evans etal., 1991). A particular concern is, however, that imposex in all whelks is not, as has been generally assumed (e.g. Foale, 1993), a specific response to TBT. Extensive studies by Bryan et al. (1986, 1987, 1988) appeared to establish that, apart from two related organotins, tri-n-propyltin and tetrabutyltin, TBT was the only compound to cause it in N. lapillus. The finding by Nias et al. (1993) that copper, and even environmental stress, could induce imposex in Lepsiella vinosa was therefore unexpected. It has wide implications if it applies to other species, and there are indications that this is the case. In particular, the results of preliminary experiments by Harding and co-workers (Davies, pers. comm.; Lfinge, pers. comm.) showed that, although development was enhanced by

Volume 30/Number 1/January 1995

WH ~ !

I

1kin

!

! lkm

a

b

lkm

L 0 1

C

_

AB lkm

e

f

Fig. 4 Imposex in whelk populations in semi-enclosed bays, sea lochs

and harbours. Data from: (a) Porirua Inlet, New Zealand (Smith & McVeagh, 1991); (b) Wellington Harbour (Smith & McVeagh, 1991); (c) Port Phillip Bay, Melbourne (Foale, 1993); (d) Loch Sween, Scotland (Davies et al., 1987); (e) Ambon Bay, Indonesia (Evans et al., in press); (f) Sullom Voe, Shetland (Bailey & Davies, 1988b). Loch Sween is used for fish farming but the other locations are centres of boating activity. In (a), (b), (c), (d) and (f): o, imposex absent or mild (RPSI < 5); e, RPSI 5-40; 0, RPSI >40. In (e): o, no imposex; e, imposex in <25% of females; O, either imposex in > 25% of females or whelks now absent.

19

Marine Pollution Bulletin RPSI

RPSI

100"

which symptoms are mild and those using whelks, in which neither the causal link between TBT and imposex, nor the specificity of the response, has been investigated. There is, nevertheless, little doubt that TBT has been the major cause of imposex in natural populations of N. lapillus and measures of it will still be valuable in monitoring recovery from it.

50• ii•e

i

i

i

Juveniles Percent

Juveniles Percent 100"

This study was sponsored by Marine Painting Forum (BMT Seatech Ltd, Wallsend, Tyne and Wear) to whom the authors are most grateful. Thanks also to Professor Bob Clark, Mr Reginald F. Bennett, Dr Reinhard L/inge, Dr Herman Schweinfarth, Dr Stewen, Dr Schumacher and Dr Julian Hunter for their comments on the manuscript and Mrs Carol Weiss for typing it.

5O

i

I

i

I

5

10

1.~

5

Distance

from

nearest

port

10

km

Fig. 5 Symptoms of imposex (RPSI) and numbers of juveniles in populations of N. lapillus plotted against distance from the nearest port or centre of boating activity. Data from (a) the north-east coast of England (Hutton, 1986); and (b) the Isle of Cumbrae, Scotland (Evans et al., 1994).

low concentrations of TBT, it also occurred in TBT-free control groups exposed solely to ethanol (the TBT solvent) or clean seawater. Each of the following 'anomalous' results can also be explained if imposex is caused by agents other than TBT: (i)

Imposex has been described in populations of N. lapillus from New England which had undetectable levels of tin in their tissues but elevated levels of copper and, to some extent, zinc (Miller & Pondick, 1984). It has also been described in L. scobina (Stewart et al., 1992), L. vinosa (Foale, 1993) and N. lapillus (Harding et aL, 1992) which had no tin in their tissues. (ii) The severity of imposex did not correlate with tin tissue burdens in studies of N. canaliculata and N. lamellosa (Bright & Ellis, 1989), L. scobina (Smith & McVeagh, 1991) and T. orbita (Foale, 1993). (iii) There was little agreement in measures of imposex when they were assessed by Wilson et al. (1993) in T. orbita and Morula marginalba at 16 sites to the north and south of Sydney Harbour. Spearman rank coefficients of correlation (rs) between RPSI for the two species, and for the percentages of females with symptoms of imposex, were 0.2706 and 0.2701, respectively; they were not significant ( p > 0 . 0 5 in both cases). Scores for T. orbita indicated that the coast south of Sydney was more contaminated than the coast north of it, but those for M. marginalba indicated that the converse was true. Conflicting results were also obtained from measures of imposex in M. musiva, T. luteostoma and Cronia margariticola from the same sites in Malaysia (Ellis & Pattisina, 1990). These results question the validity of imposex as a bioindicator of TBT pollution, particularly in cases in 20

Alvarez, M. M. S. & Ellis, D. (1990). Widespread neogastropod imposex in the northeast Pacific, implications for TBT contamination studies. Mar. Pollut. Bull. 21,244-247. Alzieu, C. (1991). Environmental problems caused by TBT in France: assessment, regulations, prospects. Mar. Environ. Res. 32, 7-17. Alzieu, C., Htral, M., Thibaud, Y., Dardignac, M. J. & Feuille, M. (1981-1982). Influence des peintures antisallisures ~ base d'organostanniques sur la calcification de la coquille de l'huitre Crassostrea gigas. Rec. Trav. Int. P~ches Marit. 45, 101-116. Alzieu, C., Sanjuan, J., Deltriel, J. P. & Borel, M. (1986). Tin contamination in Arcachon Bay effect on oyster shell anomalies. Mar. Pollut. Bull. 17, 494-498. Alzieu, C., Sanjuan, J., Michel, P., Borel, M. & Dreno, J. P. (1989). Monitoring and assessment of butyltins in Atlantic coastal waters. Mar. Pollut. Bull. 20, 22-26. Anon. (1993a). TBT pollution from ships threatens North Sea species. ENDS Report 227, 7-8. Anon. (1993b). Man's impact on ecosystems. In North Sea Quality Status Report, pp. 80-98. North Sea Task Force, Oslo and Paris Commissions, London, UK/Olsen & Olsen, Fredensborg, Denmark. Bacci, E. & Gaggi, C. (1989). Organotin inputs in harbour and marina waters from the north Tyrrhenian Sea, Mar. Pollut. Bull. 20, 290292. Bailey, S. K. & Davies, I. M. (1987). Tributyltin contamination in the Firth of Forth. Proc. R. Soc. Edinburgh B 93,561-562. Bailey, S. K. & Davies, I. M. (1988a). Tributyltin contamination in the Firth of Forth (1975-1987). Sci. TotalEnviron. 76, 185-192. Bailey, S. K. & Davies, I. M. (1988b). Tributyltin contamination around an oil terminal in Sullom Voe (Shetland). Environ. Pollut. 55, 161172. Bailey, S. K. & Davies, I. M. (1989). The effects of tributyltin on dogwhelks (Nucella lapillus) from Scottish coastal waters. J. Mar. Biol. Assoc. UK 69,335-354. Bailey, S. K. & Davies, I. M. (1991). Continuing impact of TBT, previously used in mariculture, on dogwhelks (Nucella lapillus L.) populations in a Scottish sea loch. Mar. Environ. Res. 32, 187-199. Batley, G. E., Fuhua, C., Borckbank, C. I. & Flegg, K. J. (1989). Accumulation of tributyltin by the Sydney Rock Oyster, Saccostrea commercialis. Aust. J. Mar. Freshwater Res. 40, 49-54. Beaumont, A. R. & Newman, P. B. (1986). Low levels of tributyltin reduce growth of microalgae. Mar. Pollut. Bull. 19, 294-296. Bright, D. A. & Ellis, D. V. (1989). A comparative survey of imposex in north-east Pacific neogastropods (Prosobranchia) related to tributyltin contamination, and choice of suitable bioindicator. Can. J. Zool. 68, 1915-1924. Bryan, G. W., Gibbs, P. E., Burt, G. R. & Hummerstone, L. G. (1986). The decline of the gastropod Nucella lapillus around South-West England: evidence for the effects of tributyltin from anti-fouling paints. J. Mar. Biol. Assoc. UK 66, 611-640. Bryan, G. W., Gibbs, P. E., Burt, G. R. & Hummerstone, L. G. (1987). The effects of tributyltin (TBT) accumulation on adult dogwhelks, Nucella lapillus: long-term field and laboratory experiments. Z Mar. Biol. Assoc. UK 67,525-544. Bryan, G. W., Gibbs, P. E. & Burt, G. R. (1988). A comparison of the effectiveness of tri-n-butyltin chloride and five other organotin compounds in promoting the development of imposex in the dogwhelk, Nucella lapillus. J. Mar. Biol. Assoc. UK 68,733-744. CEFIC (1994). Use of triorganotin compounds in anti-fouling paints. Results of TBT monitoring studies. Paper submitted to International Maritime Organisation Marine Environment Protection Committee, 35th Session; Agenda item 17, 7 pp. Claisse, D. & Alzieu, C. (1993). Copper contamination as a result of antifouling paint regulations? Mar. Pollut. Bull. 26, 395-397.

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