P.E. Gibbs

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 .

The effect of tributyltin upon steroid titres in the female dogwhelk, Nucella lapillus, and the development of imposex

Abstract Exposure of female Nucella lapillus to tributyltin (TBT) in seawater at a concentration of 40 ng Sn/litre led to accumulation of TBT in the tissues, and an increase in penis length compared to control animals. Investigation of the steroid concentrations by radioimmunoassay revealed a significant increase in testosterone after 28 days exposure to TBT. No significant effect was noted upon the amounts of progesterone or estradiol-17β. When testosterone was injected into female N. lapillus in the absence of TBT, penis length was found to increase significantly. These observation suggest that there may be an association between the change in testosterone titre in response to exposure to TBT and the development of imposex in the dogwhelk.

TBT-induced imposex in the dogwhelk, Nucella lapillus: Geographical uniformity of the response and effects

The imposex response of the dogwhelk, Nucella lapillus, to tributyltin (TBT) pollution has been investigated in adults taken from four UK populations geographically separated over 10° of latitude. Exposure to TBT water concentrations of c.1 and 17 ng Sn/litre over a period of 12 weeks resulted in similar levels of accumulation of TBT within the body tissues and similar increases in female penis length in all four populations. The features are imposex in N. lapillus populations in south-west Brittany are described; they follow the same pattern as found in earlier surveys of the southern England coast, including sterilisation of females, population decline and disappearance of the species close to TBT sources. The evidence of these two investigations indicates that the level of sensitivity and development of imposex as a response to TBT pollution is uniform in N. lapillus throughout its distributional range.

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.

Tributyltin-induced imposex in stenoglossan gastropods: Pathological effects on the female reproductive system

Abstract 1. 1. The imposition of male sex organs on female stenoglossan gastropods—“imposex”—is a worldwide phenomenon now known to be associated with the usage of marine antifouling paints containing tributyltin (TBT) compounds. 2. 2. The effect of the imposex response on the female reproductive system varies according to species: in some, breeding appears unaffected, whilst in others the anatomy of the oviduct may be so modified that the female is effectively sterilised. 3. 3. New evidence suggests that TBT interrupts steroid metabolism, notably the conversion of testosterone to oestradiol 17β.

A Male genital defect in the dog-whelk, Nucella lapillus (Neogastropoda), favouring survival in a TBT-polluted area

Tributyltin (TBT) pollution has exterminated populations of the dog-whelk Nucella lapillus along most of the north Kent coast (Thames Estuary) but the species survives as a small enclave around the North Foreland. Males in this enclave exhibit an unusual defect involving the non-development or partial development of the genital system: about 10% lack penes, or have undersized penes, and their gonoducts (vas deferens and prostate) are incompletely developed; in some cases, spermatogenesis appears to be retarded. Laboratory-bred animals display the same characters. This deficiency (‘Dumpton Syndrome’) is manifest also in the atypical development of male sex organs on the females (‘imposex’) induced by exposure to tributyltin (TBT). The evidence points to Dumpton Syndrome being a genetic disorder which has lessened the sterilizing effect of imposex and thereby has permitted the survival of this isolated enclave in an area of high TBT pollution.

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.

Effects of tributyltin (TBT) exposure on the reproduction and embryonic development of the bivalve Scrobicularia plana

Abstract Field and laboratory work was carried out during the summers of 1990 and 1991 on bivalves Scrobicularia plana from sites moderately-affected and relatively-unaffected by tributyltin (TBT) contamination (i.e. a mean concentration in clam tissues of 0.4 and 0.02 μg Sn g−1 dry wt, respectively). Standard cultures after artificial fertilizations with broodstock of either site did not result in dissimilar survival of embryos nor in larvae of different quality at the time of hatching. Static 48 h toxicity tests on S. plana embryos showed that an EC50 of less than the nominal 250 ng Sn litre−1 (a range of 178–198 ng Sn litre−1, as analysed) can be set for TBT independently of the origin of broodstock. The results are discussed in relation to the reported disappearance of S. plana throughout northern Europe and the simultaneous presence of toxic levels of butyltin. It is concluded that TBT has probably reduced the recruitment into some UK clam populations by preventing the successful development of a significant proportion of their embryos.