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

Author(s):  
P. E. Gibbs ◽  
P. L. Pascoe ◽  
G. R. Burt

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.

Author(s):  
P. E. Gibbs ◽  
G. W. Bryan

The development of male characters, notably a penis and a vas deferens, on the female (the phenomenon of ‘imposex’) of the dog-whelk, Nucella lapillus, is described. Three stages are recognized: an ‘early’ stage involving the formation of a vas deferens and a small penis, an ‘intermediate’ stage characterized by the enlargement of the female penis to a size approaching that of the male and a ‘late’ stage during which the female opening (vulva) is occluded by overgrowth of vas deferens tissue. This blockage of the pallial oviduct prevents the release of egg capsules and renders the female sterile. The extent and cause of such reproductive failure is evident from the high incidence of females containing aborted capsules in declining populations close to sources of tributyltin (TBT) contamination. These same populations comprise fewer females than expected and it would appear that the accumulation of aborted capsules within the pallial oviduct eventually causes the premature death of the female.


Author(s):  
G. W. Bryan ◽  
P. E. Gibbs ◽  
G. R. Burt

Populations of the common dog-whelk Nucella lapillus (L.) are declining or have already disappeared at many sites on rocky shores around the United Kingdom (Bryan et al. 1986). There is conclusive evidence that this is caused mainly by tributyltin (TBT) compounds leached from ships' antifouling paints (Bryan et al. 1987). These compounds impose male sexual characters (or imposex) on female N. lapillus. Other stenoglossan gastropods including Nassarius obsoletus Say (Smith, 1981a) and Ocenebra erinacea (L.) (Féral & Gall, 1982) are similarly affected by TBT. The intensity of expression of imposex in N. lapillus can generally be related to the sea water concentration of TBT. The appearance of a small penis and the partial development of a vas deferens first occurs at TBT concentrations below 0.5 ng/1 (as tin), although reproduction appears to be unaffected at this level. At 1–2 ng Sn/1 penis size is markedly increased and in some females proliferation of vas deferens tissue overgrows the genital papilla, thus sterilizing the animal. At slightly higher concentrations virtually all females become sterilized and at around 10 ng Sn/1 oogenesis is suppressed and spermatogenesis initiated (Gibbs, Pascoe & Burt, 1988). Since development is direct and there is no planktonic stage, N. lapillus has a very limited capacity for dispersion: thus the sterilization of females heralds the almost certain decline of so affected populations (Gibbs & Bryan, 1986).


Author(s):  
S.K. Bailey ◽  
I.M. Davies

The common dogwhelk (Nucella lapillus) is a dioecious species. However, on exposure to low concentrations (<1 ng I-1, Gibbs et al., 1987) of tributyltin (TBT) females develop certain male sexual characteristics, notably a penis and vas deferens. This phenomenon, first reported by Blaber (1970) in dogwhelks from the Plymouth area, and later termed 'imposex' (Smith, 1981), is now recognised as the most sensitive and straightforward way to identify contamination of coastal areas by TBT. The degree of imposex may be readily quantified as the relative penis size index (RPSI), which expresses the relative bulk of the penes in females and males from a given sample. It is calculated as (mean cubed female penis length/the mean cubed male penis length) x 100% (Gibbs et al., 1987). Gibbs et al. (1987) have examined the development of imposex in greater detail, and have divided the process into six stages (known as the vas deferens sequence, or VDS) based upon the degree of development of the vas deferens and penis in the female animal. This classification enables an assessment to be made of the reproductive ability of an animal. Stages 1 to 4 show a progressive development of the penis and vas deferens. At a VDS of 5, vas deferens tissue proliferates over the opening of the reproductive tract, blocking it, and subsequently causing sterility due to the inability of the animal to release egg capsules. Aborted egg capsules then gradually accumulate in the capsule gland (stage 6). The vas deferens sequence index, VDSI, is the mean VDS in a given sample of females.


Author(s):  
G. W. Bryan ◽  
P. E. Gibbs ◽  
G. R. Burt ◽  
L. G. Hummerstone

Populations of the gastropod, Nucella lapillus (L.), normally one of the commonest of rocky-shore macroinvertebrates, have recently suffered from declining numbers at many sites along the south coast of England. Bryan et al. (1986) showed that these declining populations exhibited a high degree of imposex (the induction of a penis and vas deferens in females) and that imposex was almost certainly caused by tributyltin (TBT) compounds leached from ships' antifouling paints. Evidence implicating TBT compounds in the development of imposex included: (1) a good relationship between the degree of imposex and the proximity of affected populations to harbours and marinas; (2) in Plymouth Sound, the degree of imposex increased dramatically between its discovery in 1969 (Blaber, 1970) and 1985, thus coinciding with the introduction and increasing usage of TBT-based paints; (3) tissue concentrations of tin as TBT increased consistently with the degree of imposex; (4) animals transplanted from a ‘clean’ area to a harbour site absorbed TBT and developed imposex; (5) preliminary experiments showed that imposex was induced by exposure to 20 ng/1 of tin as TBT leached from a TBT-based paint; (6) TBT is implicated in the induction of imposex in other stenoglossan gastropods including Nassarius obsoletus (Say) (Smith, 1981) and Ocenebra erinacea (L.) (Féral & Gall, 1982).


Author(s):  
P.E. Gibbs ◽  
J.C. Green ◽  
P.L. Pascoe

In the summer of 1995 a massive kill of the dog-whelk, Nucella lapillus, occurred in Bude Bay on the north Cornish coast. High mortality was detectable along 12 km of shoreline. The only other intertidal species affected appeared to be another neogastropod, Ocenebra erinacea. The cause of the kill is unknown but the evidence suggests that it occurred in early July following an extended period of warm, calm weather in June. Possible causes of this event are discussed: algal toxicity may have been responsible since an algal bloom was detected offshore in July in the area. Laboratory experiments exposing gastropods to different species and concentrations of microalgae, designed to test whether N. lapillus is more sensitive than Monodonta lineata and Littorina littorea, gave inconclusive results. No comparable kill has occurred in the Bude area for at least 20 y, but it is suggested that nutrients from a newly-constructed, offshore sewage outfall may now stimulate local algal bloom development during calm weather periods.


2019 ◽  
Vol 99 (7) ◽  
pp. 1601-1614
Author(s):  
J. M. Ruiz ◽  
B. Carro ◽  
N. Albaina ◽  
L. Couceiro ◽  
M. Quintela ◽  
...  

AbstractWe have monitored tributyltin (TBT) pollution in Galicia (NW Spain) for more than a decade by means of assessing gastropod imposex in populations of Nucella lapillus (N ≥ 34) and Tritia reticulata (N ≥ 18) at regular intervals. Several thousand specimens were processed to obtain their shell height (SH), penis length (PL) and vas deferens sequence (VDS); imposex indices (including the VDS index, VDSI) were subsequently calculated. The regional mean SH of both females and males has not changed significantly in either species throughout the study. This also applies to the mean male PL in N. lapillus, but male T. reticulata penises surprisingly enlarged. On the contrary, the regional mean female PL (MFPL) and all imposex indices significantly decreased in both snails. Results confirm previous conclusions based on the chemical analyses of tissues and partial imposex observations. In addition, the close correlations between MFPL and VDSI show some potential applications to TBT biomonitoring.


2011 ◽  
Vol 6 (1) ◽  
pp. 84-90 ◽  
Author(s):  
Zhi-Hua Li ◽  
Vladimir Zlabek ◽  
Roman Grabic ◽  
Ping Li ◽  
Tomas Randak

AbstractThe aim of this study is to investigate the toxic effect of PCZ, a triazole fungicide commonly present in surface and ground water, on the ROS defense system and Na+-K+-ATPase in gills of rainbow trout exposed to sublethal concentrations (0.2, 50 and 500 μg L−1) for 7, 20 and 30 days. After prolonged exposure of PCZ at higher test concentrations (50 and 500 μg L−1), oxidative stress was apparent as reflected by the significant higher ROS levels in fish gill, as well as the significant inhibition of SOD and CAT activities. In addition, Na+-K+-ATPase activities were significantly lower than those of the control with increasing PCZ concentration and prolonged exposure period. The results of this study indicate that chronic exposure to PCZ has altered multiple physiological indices in fish gill; however, before these parameters are used as unique biomarkers for monitoring residual pharmaceuticals in aquatic environments, more detailed laboratory experiments need to be performed.


Author(s):  
P.E. Gibbs

Laboratory breeding of the dog-whelk, Nucella lapillus, has established that the male-sterilizing Dumpton Syndrome (DS)—underdevelopment, or non-development (aphally), of the penis, incomplete formation (non-closure) of the vas deferens, resulting in a split prostate—can be readily observed in male F1 progeny. Cultivated under high ambient concentrations of the antifouling agent tributyltin (TBT), DS-carrying females can be recognized by their lesser degree of masculinization (imposex): sterilization is thereby avoided. When Dumpton females are crossed, under high ambient TBT, with individuals from a non-DS-affected population (Bude, North Cornwall) DS is absent from both sexes. Crosses of these F1 progeny result in F2 progeny exhibiting the classic DS symptoms in both sexes. A Mendelian mechanism for DS inheritance is suggested by the data.


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