Dumpton Syndrome reduces the tributyltin (TBT) sterilising effect on Nucella lapillus (L.) by limiting the development of the imposed vas deferens

2002 ◽  
Vol 54 (3-5) ◽  
pp. 657-660 ◽  
Author(s):  
M Quintela ◽  
R Barreiro ◽  
J.M Ruiz
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.


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.


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.


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):  
P. E. Gibbs

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.


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):  
M. Huet ◽  
N. Le Goïc ◽  
P.E. Gibbs

Most neogastropod species exhibit masculinization of the female when subject to tributyltin (TBT) pollution (a process known as ‘imposex’). To date, the dog-whelk Nucella lapillus is seemingly unique in having a genetic deficiency (termed Dumpton syndrome or DS) that disrupts the development of normal male sex organs, its presence being readily recognizable by the underdevelopment, or non-development (aphally), of the penis, and incomplete formation (non-closure) of the vas deferens, causing a split prostate. In highly contaminated conditions, female carriers of DS can be identified by a lesser degree of masculinization (notably aphally): they escape sterilization caused by the advanced stages of imposex. To date, DS has only been reported in areas with high TBT pollution which induces sterilization of normal females (i.e. non DS-affected females). DS is now, for the first time, observed at some locations where present TBT levels are low and some normal females lack penis development. In such conditions it is not possible to discriminate normal from DS-affected females using aphally. As DS-affected females must be discarded from the calculation of the imposex bioindicators to monitor TBT pollution, indirect tools such as molecular probe are now needed to further survey those areas where DS and TBT pollution may interact as, for example, in south-west Brittany.


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

SynopsisCommon dogwhelks (Nucella lapillus) show a characteristic response to exposure to tributyltin compounds. Females develop male sexual characteristics, a phenomenon termed imposex. Dogwhelks have been collected for assesment of imposex from sites throughout Sullom Voe and Yell Sound in 1987, 1990 and 1991.Results of the 1991 survey have indicated that dogwhelks were completely absent from the terminal area, on the promontory of Calback Ness. The degree of imposex was highest in the population from Kames, the site closest to the terminal. Juveniles were completely absent from this site. Incidence of imposex was high in populations throughout the Voe and 91% of the females examined from within the Voe were reproductively unviable due to blockage of their reproductive tracts with vas deferens tissue. Outside the Voe, in the well flushed waters of Yell Sound, imposex was much lower, but only fell to levels associated with populations from areas distant from tributyltin (TBT) contamination in the two most northerly sites surveyed.Results of the survey have indicated that activities associated with the oil terminal are the source of TBT contamination to the area, and that contamination arising from the terminal operations has not only affected dogwhelks in Sullom Voe, but populations throughout Yell Sound.Comparison of the imposex levels from 1987 and 1990 data indicates that the reproductive capacity of females has progressively declined and that populations within the Voe are gradually being eliminated. Forty-six percent of females sampled from populations within the Voe were sterile in 1987, compared to 65% in 1990, and 91% in 1991. In 1987, both adult and juvenile dogwhelks were present in the jetty area, although 94.5% of the females were sterile. In 1990, juveniles were absent from this area, and all females were sterile. No dogwhelks were found in the terminal area during the 1991 survey and, at Kames, the next closest site, juveniles were absent.


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.


2011 ◽  
Vol 46 (1) ◽  
pp. 74-86 ◽  
Author(s):  
C. P. Titley-O'Neal ◽  
B. A. MacDonald ◽  
É. Pelletier ◽  
R. Saint-Louis

Dogwhelks (Nucella lapillus), a universal bioindicator of tributyltin (TBT) pollution, were used to determine butyltin distribution in three Atlantic Canada harbours previously surveyed between 1995 and 2006. N. lapillus were analysed for the presence of TBT and its degradative products while imposex incidence and severity were compared with previous surveys to assess the efficacy of the Canadian regulations on TBT. Imposex was observed at two harbours that had dogwhelks, but not at surrounding reference sites. When comparing results with previous surveys in the same geographic area, there appears to be some improvement of affected N. lapillus populations, suggesting that the 1989 Canadian regulations have been effective in decreasing imposex severity for most sites as measured by the vas deferens sequence index (VDSI), but not the occurrence of imposex. The highest butyltin tissue concentration (63.75 ng Sn g−1, dry wt) was detected in imposex-affected females from Red Head in Saint John Harbour (New Brunswick), which is adjacent to an area frequented by large oil tankers that, under the 1989 regulations, are legally allowed to use TBT antifouling paint. This study is the first to illustrate a significant correlation between TBT levels and imposex on a spatial scale in Atlantic Canada.


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