G. R. Burt

The Decline of the Gastropod Nucella Lapillus Around South-West England: Evidence for the Effect of Tributyltin from Antifouling Paints

A survey of the gastropod Nucella lapillus around the south-west peninsula of England has revealed that the incidence of ‘imposex’, the induction of male sex characters in the female, is widespread, that all populations are affected to some degree and that the phenomenon is most prevalent along the south (Channel) coast. Populations close to centres of boating and shipping activity show the highest degrees of imposex, especially those within the vicinities of the Helford, Fal, Salcombe and Dart estuaries and in Plymouth Sound and Tor Bay. Within Plymouth Sound the degree of imposex increased markedly between 1969 and 1985, coinciding with the introduction and increasing usage of antifouling paints containing tributyltin (TBT) compounds.

The use of the dog-whelk, Nucella lapillus , as an indicator of tributyltin (TBT) contamination

The term ‘imposex’ was coined by Smith (1971) to describe the superimposition of male characters onto unparasitized and parasitized females of gonochoristic gastropods. In Nassarius obsoletus (Say) the development of imposex results in the female having one or more of the following characters: (1) a penis with a duct leading to (2) a vas deferens which passes back to the ventral channel of the capsule gland and (3) convolution of the normally straight gonadial oviduct (Smith, 1980). Imposex in the similarly gonochoristic Nucella lapillus (L.) was first noted by Blaber (1970) who found females with penis-like outgrowths in Plymouth Sound populations. Subsequent studies (Bryan et al. 1986; Gibbs & Bryan, 1986) have demonstrated that the incidence and intensity of imposex have since increased markedly in the same populations and that the phenomenon is widespread around south-west England.

Sex Change in the Female Dog-Whelk, Nucella Lapillus , Induced by Tributyltin from Antifouling Paints

Imposex, the development of a penis and vas deferens in the female (Smith, 1971) is known to occur in over 30 species of marine gastropods but, to date, in only one species has this syndrome been demonstrated to have a serious deleterious effect. This species is the dog-whelk, Nucella lapillus L. Both field and laboratory observations have provided conclusive evidence that imposex in N. lapillus is initiated by tributyltin (TBT), used as a biocide in antifouling paints, at concentrations in water of less than 1 ng Sn/1. This feature is manifest in the widespread occurrence of imposex even in areas far removed from centres of boating activity (see Bryan et al. 1986). Imposex appears to have little effect on the reproductive biology of N. lapillus until this syndrome is developed to its fullest extent when it sterilises the female because the pallial oviduct becomes occluded by vas deferens tissue thus preventing expulsion of the egg capsules (Gibbs & Bryan, 1986). Laboratory experiments have indicated that this condition, found in females close to harbours and marinas, may prevail after prolonged exposure during the first few years of life to TBT levels as low as 2 ng Sn/1 (Gibbs et al. 1987). Of six organotin compounds tested by Bryan, Gibbs & Burt (1988), tributyltin chloride proved the most effective in promoting imposex in N. lapillus .

Bioavailability and effects of sediment-bound TBT in deposit-feeding clams, Scrobicularia plana

Concentrations of tributyltin (TBT), dibutyltin (DBT), inorganic and total tin have been measured in water, sediments and deposit feeding clams, Scrobicularia plana, from 25 estuarine locations in England and Wales, in order to compare the bioavailability of different forms of the element. Abnormally high tin values in Scrobicularia from harbours and areas of high boating activity testify to the high bioaccumulation potential of organotins, notably TBT derived from anti-fouling paints, relative to inorganic tin. Infaunal deposit-feeding bivalves consistently contain higher concentrations of TBT than other benthic organisms indicating that sediments may be an important route for uptake. Significant correlations between sediment TBT values and residues in clams such as S. plana (r = 0·81, p < 0·001) support this hypothesis. Direct evidence of the bioaccumulation of sediment-bound TBT is provided from laboratory experiments in which Scrobicularia were exposed to TBT in water and in sediments, either separately or in combination. The results of these experiments clearly demonstrate a predominantly particulate component for TBT uptake in clams. The kinetics of TBT accumulation and elimination were studied in Scrobicularia exposed to sediments containing 0·3 and 1·0 μg/g TBT (as tin). Equilibrium concentrations in tissue are approached after 40 days. Sediments containing 10 μg/g TBT are acutely toxic to S. plana, although such concentrations are only likely to occur close to dockyards and large marinas. Preliminary laboratory and field observations suggest however, that clam populations could be affected at TBT concentrations in sediments of 0·3 μg/g and possibly lower.

An assessment of the gastropod, Littorina littorea , as an indicator of heavy-metal contamination in United Kingdom estuaries

Preliminary determinations of heavy metals in winkles Littorina littorea along a concentration gradient in the Fal Estuary suggested that whole body concentrations might be related to those of the water. When animals were transplanted to this heavily contaminated estuary, changes in tissue concentrations of As, Co, Cu and Zn were largely complete after 2 months. Relations between the winkle and water concentrations may be indirect since its algal diet is thought to be the main source for most heavy metals. Data from a large number of United Kingdom estuaries were used to compare concentrations of 12 metals in L. littorea with those of the brown seaweed Fucus vesiculosus which forms part of its diet. Very significant relations were found for Ag, As, Cd and Pb, suggesting that since concentrations in the seaweed probably reflect those of the surrounding water, so also do those of the winkle. However, concentrations of Ag in the animal also appeared to be influenced by dietary Cu levels. In addition, significant relations between the two species were found for Cu, Fe, Hg and Zn, but the slopes were shallow, perhaps indicating regulation by the winkle. For Cr and Mn relations were not very significant and, for Co and Ni, concentrations in the winkle appeared to be influenced by those of Cu and Zn. Compared with concentrations in L. littorea , those of L. littoralis from the same site were generally higher whilst in L. saxatilis they were usually of the same order or lower. In assessing the winkle as an indicator of metal contamination the present results have been combined with those of other workers to produce comparisons between most estuaries in England and Wales. It is concluded that whilst the winkle is a useful indicator for Cd and a few other metals, it is certainly not a perfect indicator organism.

Nassarius reticulatus (Nassariidae: Gastropoda) as an indicator of tributyltin pollution before and after TBT restrictions

Between 1984 and 1993, levels of imposex (the induction of male characters including a penis on females) were measured in gastropods Nassarius (Hinia) reticulatus (L.) at localities in south-west England. Since tributyltin (TBT) was thought to cause imposex, concentrations in tissues and sea-water were also determined. Measurements made prior to the restriction of TBT usage in 1987 showed that intensities of imposex were related to TBT levels in females. Tissue concentrations were also related to those of sea-water and concentration factors (dry tissue/water) were approximately 30,000 at 10 ng Sn I -1 and 75,000 at 1 ng Sn I -1 . Penis development in females was initiated at about 1 ng Sn I -1 and in this respect JV. reticulatus appears less sensitive to TBT than the dog-whelk Nucella lapillus . As result of the TBT restrictions, concentrations in sea-water and tissues at some of the more polluted sites decreased by factors of 5–10 times between 1987 and 1993. However, population imposex declined very slowly. This was attributed to the longevity of the snails, the slow decline of penis-length in older females and the limited recruitment of less-affected females. It was concluded that N. reticulatus is a useful alternative to N. lapillus as an imposex-based TBT indicator at contaminated sites. However, when environmental TBT concentrations are declining fairly rapidly, analysis of N. reticulatus tissues provides a far better indication of change than measurements of population imposex.

Uptake and transformation of 14C-labelled tributyltin chloride by the dog-whelk, nucella lapillus: Importance of absorption from the diet

Abstract The importance of the diet as a source of tributyltin (TBT) in Nucella lapillus was studied using [14C]tributyltin chloride. In N. lapillus provided with prelabelled mussels, Mytilus edulis, in labelled water (mean 20·5 ng/litre TBT) the rate of accumulation of total 14C was 2–3 times that in unfed animals. Owing to its degradation in the tissues of both fed and unfed animals, concentrations of [14C]TBT tended to reach a plateau after only 28 days. However, total concentrations of 14C were still increasing after 49 days. Under experimental conditions (15°C, ample food, no disturbance) the diet accounted for about 50% of the body burden of TBT in N. lapillus after 49 days exposure: concentration factors (dry tissue/water) for [14C]TBT in both male and female N. lapillus were similar at about 60 000 in fed and 30 000 in unfed animals. It is concluded that the diet may contribute less than half of the body burden of TBT found in natural populations subjected to life-long exposure.

Zinc copper and chlorophyll-derivatives in the polychaete Owenia fusiformis

An earlier study of metals in the polychaete Owenia fusiformis showed that individuals within intertidal populations were remarkably variable in terms of whole-body concentrations of zinc and copper. Four populations have now been studied, two in south Cornwall (Fal Estuary and Par Sands) and one each in east Devon (Torre Abbey Sands) and north Brittany (Greve de St Michel). Investigations of the distributions of zinc and copper within the body have demonstrated that consistently zinc is concentrated in the middle body whilst copper increases to a maximum posteriorly. Zinc is accumulated in the mid-gut cells in the form of numerous spherules, 1–2 μm in diameter: X-ray microanalysis shows these to be largely composed of zinc phosphate but containing also magnesium, calcium and iron, together with sulphur and chlorine. Viewed under the microscope the spherules are greenish due to a pigment identified by high performance liquid chromatography absorption scanning as a pheophorbide-like chlorophyll-degradation product. In contrast, copper is widely distributed throughout the body and much is deposited as small granules, 0.2–0.3 μm in diameter, in laminar groupings in hypodermal and peri-intestinal tissues. The identity of the green pigment responsible for the characteristic body colour of O. fusiformis has not been specifically determined but it appears to have a copper basis since dark-green tissues have a significantly higher copper content than those with a light-green colour. The possible role of chlorophyll degradation products in zinc and copper uptake is discussed.