Imposex - Marine online assessment tool

Following bans on the use of tributyltin and other organotins there has been a marked improvement in the reproductive condition of dog whelks in the UK. Although there are still some stations that exceed the safe environmental limits for imposex, the majority of stations pass the UKMS target for this indicator.

Background

Antifouling paints are widely used on marine vessels and other submerged structures to prevent the growth of unwanted marine organisms on surfaces (Figure 1). Since the late 1960s, antifouling/biocide paints containing tributyltin (TBT) have been used to prevent the attachment of undesired algae and other organisms on submerged surfaces. By the mid-1980s, TBT-based antifouling paints used on small craft operating in waters near commercial shellfish beds were identified as the cause of shell chambering and the consequent poor growth in oyster stocks.

Image of testing metal in a shipyard for antifouling material. Different sections are painted in various shades of red and blue.

Figure 1: Patch testing antifouling material. © MAPIEM, University of Toulon

TBT is toxic to many marine organisms at very low concentrations and is unequivocally linked to reduced reproductive performance in several snail species (Figure 2).

Since the mid-1980s, a range of national and international measures has resulted in the phasing out of paints containing TBT in the OSPAR Maritime Area. In 2008, a global ban on the use of organotins in antifouling paints on all marine boats and ships, regardless of size, came into effect.

Image of the marine gastropod Nucella lapillus (the dog whelk) in its marine environment on a rock.

Figure 2: Tributyltin affects many organisms, but marine gastropods, such as the dog whelk, Nucella lapillus (L.) are among the most sensitive. © Gordon Fletcher

Following TBT exposure, the entire female genital system of some marine snail species (gastropods) is conserved, but male sexual organs develop on top of them (Smith, 1981). This is termed ‘imposex’. An OSPAR indicator has been developed to measure the intensity of imposex within the OSPAR Maritime Area using the Vas Deferens Sequence (VDS). Although TBT ultimately affects many organisms, marine gastropods such as the dog whelk, are among the most sensitive, making this an ideal bioindicator species for monitoring imposex intensity through VDS.

Further information

Organotin compounds are based on tin with hydrocarbon substituents; examples are tributyltin (TBT) and its degradation metabolites dibutyltin (DBT) and monobutyltin (MBT). They were used as insecticides, bactericides, and fungicides since the 1920s, but in the late 1960s it was discovered that they were very efficient at preventing biofouling (growth of organisms) on boat hulls.

Research on the toxicity of TBT in the 1970s focused on lethal, short-term effects, not on sub-lethal, longer-term effects, and thereby failed to connect TBT with the chronic phenomenon of imposex, which had been described in American and English harbours from 1970. Imposex and intersex are known as the condition whereby female marine snails (gastropods) develop male sexual characteristics, with individuals affected to varying degrees. The level of imposex can be less severe, such as development of vas deferens (the male sperm ducts), or more severe, where male reproductive tissue covers the female organs and renders the snail sterile. In for instance Tritia reticulata, sterilisation can also happen due to internal modifications of the organs (e.g., vulva, vagina, oviduct) although there is still scarce information in the literature on this.

Research on TBTs were for many years hampered by the inability to estimate the concentrations of TBT in the environment. The link between TBT and imposex/intersex was first discovered in France, where the oyster industry experienced massive mortality of oyster larvae and shell chambering in adults, which consequently resulted in large losses in the oyster industry in the late 1970s. In 1982, France was the first country to regulate TBT by banning the use of TBT paints on small vessels (<25 m).

In the UK, a more voluntary approach was followed, including controls on sales, and issuing guidelines for the use of TBT. The UK also set an environmental target of 20 ng/L TBT in marine waters, which at the time was considered to be sufficiently protective for marine biota. However, during the 1980s it was found that sterilization of female dog whelks occurs at concentrations as low as 3-5 ng/L TBT (Gibbs and others., 1988). In contrast, summertime concentrations of TBT regularly exceeded 100 ng/L. As a result, dog whelks disappeared in many areas as they could no longer reproduce.

Areas such as Arcachon Bay in France did in fact recover. However, the recovery of dog whelk populations was still slower than expected through the 1990s. Studies at the Sullom Voe oil terminal in Shetland conducted in 1988 (Bailey and Davies, 1988) had shown that the environment received significant inputs of TBT from TBT-coated oil tankers. Several studies indicated that the shipping industry caused imposex in several snail species in offshore waters. Moreover, there is evidence that TBT damage is not limited to snails or even molluscs. TBT has also been measured in other non-target species of sea mammals such as bottlenose dolphins and has been linked to mortality events. In the South-North Sea, it has been suggested that the breakdown of the commercial catches of the crustacean Crangon crangon in 1990-1991 was caused by endocrine disruption as a consequence of a high body burden of TBT (Parmentier and others., 2019).

By the mid-1990s, it was also realised at the political level that a worldwide phase-out of TBT use on ships should be targeted. This resulted in the International Convention on the Control of Harmful Antifouling Systems on Ships, which was adopted in 2001 and entered into force in 2008. This has been adapted by most coastal countries globally, including all OSPAR countries. However, there are still countries where TBT is not banned, TBT is still manufactured in the USA for instance and is available on the market (Uc-Peraza, 2022).

There are also some freshwater sources of TBT. It was widely used as a wood preservative (now banned) and has been found in guttering and drainpipes.

Assessment method

In assessing a suite of marine contaminants both ‘relative’ and ‘absolute’ aspects have been analysed:

‘trend assessment’ or spatial distribution assessment to focus on relative differences and changes on spatial and temporal scales, provides information about the rates of change and whether contamination is widespread or confined to specific locations; and

‘status assessment’ of the significance of the (risk of) pollution, defined as the status where chemicals are at a hazardous level, usually requires assessment criteria that take account of the possible severity of the impacts and hence require criteria that take account of the natural conditions (background concentrations) and the contaminants’ ecotoxicology. For example, Environmental Assessment Criteria (EAC) are tools in this type of assessment.

Methods for analyses of imposex trends and status

Tributyltin (TBT) is on the OSPAR List of Chemicals for Priority Action (OSPAR, 2004). Monitoring of TBT concentrations in sediment, and its biological effects, are mandatory elements of the Co-ordinated Environmental Monitoring Programme (CEMP) (OSPAR, 2010). Thus, TBT differs from the indicators for other compounds, which are only defined as concentrations of the harmful compound in the animal's tissues.

Technical Annex 3 to the JAMP Guidelines (OSPAR, 2008) sets out the guidance for monitoring TBT-specific biological effects (imposex/intersex) in the gastropod species Nucella lapillus (dog whelk), Tritia reticulata (netted dog whelk, formerly known as Tritia nitida or Nassarius reticulatus) , Buccinum undatum (common whelk) and Neptunea antiqua (red whelk). In the UK all monitoring stations are of Nucella lapillus (dog whelk).

Location of monitoring sites

Imposex is currently monitored at 70 sites in dog whelks in the UK (Table 1, Figure 3). Monitoring sites were selected using a range of approaches, although there is an emphasis on monitoring sites which are in, or near, harbours, ports, and marinas.

Table 1: Number of monitoring sites used to assess status and temporal trends of imposex in dog whelks.

UKMS subregion	Biogeographic region	Number of sites
Greater North Sea	Northern North Sea	11
Greater North Sea	Southern North Sea	0
Greater North Sea	E Channel	5
Celtic Seas	Scottish Continental Shelf	21
Celtic Seas	Minches & W Scotland	3
Celtic Seas	Irish Sea	22
Celtic Seas	W Channel & Celtic Sea	8

Periodically (typically every 1-4 years), the degree of imposex is measured using the Vas Deferens Sequence (VDS), a seven-stage measurement based on the degree of development of a penis and a vas deferens (male primary sex organs) onto females (Table 2). VDS = 0 indicates normal genitals, VDS = 5, and VDS = 6 indicates that the female is incapable of reproducing.

Table 2: Stages of imposex development in females and associated Vas Deferens Sequence (VDS) scores.

Characteristics of female genitals	Vas deferens Sequence (VDS)
Imposex is not evident	0
Vas deferens development is evident at the site of the vulva	1
A penis primordium is evident behind the right eye tentacle	2
Vas deferens has developed from the base of the penis (inside which a penile duct is already visible) but does not connect with the vulva	3
Vas deferens is completely developed (continuous from the penis to the vulva)	4
Vas deferens tissue proliferates over the vulva opening, rendering the female incapable of breeding	5
Egg capsules that cannot be released by vulva occlusion form a solid mass within the capsule gland	6

The VDS index (average VDS) is shown for all stations in OSPAR's contaminants assessment tool OHAT (https://dome.ices.dk/ohat/?assessmentperiod=2023).

Imposex status

Two assessment criteria are used to assess imposex in gastropods (Table 3): Background Assessment Criteria (BAC) and Environmental Assessment Criteria (EAC). Both criteria are based on the formerly used imposex classes. BACs are an aspirational ultimate objective to achieve the background level which naturally occur in the marine environment and whilst not a UKMS target, the status and trend results were used to examine progress towards this objective. Mean imposex values significantly below the BAC are said to be near background, and values below the EAC indicate no chronic effects of TBT on snails. Imposex assessment criteria are species specific, both criteria are available for dog whelks (Table 3).

Table 3. Background Assessment Criteria (BAC) and Environmental Assessment Criteria (EAC) for Vas Deferens Sequence (VDS) measurements.

Measure	Species	Common name	BAC	EAC
VDS	Nucella lapillus	Dog whelk	0.3	2.0

Meta-analysis of imposex status and trends

The meta-analyses summarise status and temporal trends for each assessment area, based on monitoring site-wise estimates. For the meta-analysis, a selection of time series are used:

For trends, baseline stations were excluded, but both representative and impacted sites were included. This is different to the contaminants and reflects the fact that much of the imposex monitoring is focused on harbours (i.e., impacted sites, or sites that were impacted in the past).

For status, all types of stations were used (baseline, representative, and impacted), as for contaminants.

Assessment areas with at least three monitoring sites with good geographic spread (the minimum number that can be considered to provide an evidence base at the biogeographic regional level)

There are at least three years of data, and there is at least one year with data in the period 2016-2021.

Estuarine sites were included in the assessment (this is different to other UKMS 2024 contaminant assessments).

The status of each time series is summarised by two values: (1) the ratio between the estimated mean VDS in the final monitoring year and the EAC (this is modelled on the square root scale to better satisfy the distributional assumptions, but is presented on the original scale for interpretation), and (2) the ratio between the estimated mean VDS in the final monitoring year and the BAC.

Subsequently, these values were summarised by assessment area using meta-analysis. Assessment area status relative to the EAC is assessed by fitting the following linear mixed model by restricted maximum likelihood (McCullagh and Nelder, 1989):

Response: status (sqrt(mean VDS / EAC));

Fixed model: biogeographic region

Random model: status estimation variation + residual variation.

Imposex temporal trends

The trend in each time series is summarised by the estimated odds ratio of the VDS of an individual whelk being above the EAC in a given year relative to the previous year. Values of 1 indicate no trend; i.e., the odds of an individual being above the EAC in a given year are the same as in the year before. Values <1 indicate that the odds of being above the EAC in a given year are lower than in the year before, so there is a decline in the level of imposex. Conversely, values >1 indicate an increase in the level of imposex. Odds ratio, rather than log odds ratio, was used because a few time series with extreme trends have less influence on the odds ratio scale. Time series with individual measurements were assessed for trends if there were at least three years of data (not necessarily consecutive years).

Regional trends are assessed by fitting the following linear mixed model by restricted maximum likelihood (McCullagh and Nelder, 1989):

response: trend (odds ratio).

fixed model: OSPAR contaminants assessment area.

random model: trend estimation variation + residual variation.

The fixed model means that a separate trend is estimated for each biogeographic region. The random model has two terms:

trend estimation variation, i.e., the variation in the trend estimates from the analysis of the original time series, assumed known and fixed; and

residual variation, i.e., the variation that cannot be explained by any of the fixed effects or the other random effects.

Figure 3: Monitoring sites used to assess tributyltin effects in dog whelks in each UK MS region (dark lines) and biogeographic subregion (light lines). All sites have sufficient data to assess both status and trends.

Methodological improvements

For the UKMS 2024 and 2018 assessments, a meta-analysis was used to synthesise the individual time series results and provide an assessment of status and temporal trends at the assessment area level. Meta-analyses take into account both the estimate of status or trend in each time series and the uncertainty in that estimate, and consequently, provide a more objective regional assessment. However, the 2018 results were presented as percentage of stations in each UKMS subregion below the EAC. Here, in addition to this, the regional assessment is also included in the main focus of the results which is in keeping with the other UKMS and OSPAR Quality Status Report contaminant assessments.

Also, fewer sites are included in the UKMS 2024 assessment (70) compared to UKMS 2018 (110). This is because the number of sites included in the monitoring programme was significantly reduced after 2010 as imposex had significantly declined in the UK. Sites sampled in 2010 would have been within the required time period for the UKMS 2018 assessment (2010 – 2015) but are now out with the time period required for this assessment (2016 – 2021).

Results

Findings in the 2018 UKMS Assessment

The 2018 UKMS assessment for imposex concluded that imposex occurrence was declining and was generally below the UK target threshold which measures whether adverse effects of tributyltin occur in marine snails (Nicolaus and others. 2018). For the Greater North Sea and Celtic Seas, 68% and 89%, respectively, of the assessments were significantly below the Environmental Assessment Criteria (Figure 4). All regions assessed showed significant downward trends.

Figure 4: Proportion of status assessments in each category by UKMS subregion in UKMS 2018 and UKMS 2024 Assessments. The number of sites in each category is included in brackets. Light Blue: the mean VDS is significantly below the Background Assessment Criteria (BAC) (p < 0.05). Dark Blue: the mean VDS is significantly below the Environmental Assessment Criteria (EAC) (p < 0.05) but not the BAC. Red: the mean VDS is not significantly below the EAC (p > 0.05).

2024 UKMS Assessment Results

Imposex in dog whelks was assessed at 70 locations from six UK biogeographic regions (Figure 5). The data used in the assessment was collected between 2004 and 2021. For regional assessment, only biogeographic regions with a minimum of three suitable stations with a reasonable geographic spread were included. There was insufficient data for regional analysis of the Scottish Continental Shelf.

Figure 5: Status and trends of imposex in dog whelks at each monitoring site for 2024 assessment period. Light blue: the mean VDS is significantly below the Background Assessment Criterion (BAC) (p < 0.05). Dark blue: the mean VDS is significantly below the Environmental Assessment Criterion (EAC) (p < 0.05) but not the BAC. Red: the mean VDS is not significantly below the EAC (p > 0.05). Circle: no significant change in mean VDS (p > 0.05). Downward triangle: significant decrease in mean VDS (p < 0.05).

Status assessment

The degree of imposex was categorised by Vas Deferens Sequence (VDS) stages and compared to OSPAR Background Assessment Criteria (BAC) and Environmental Assessment Criteria (EAC). The BAC determines if observed VDS is at background or elevated and EAC identifies if it is causing significant harm. An average VDS below the EAC indicates an acceptable health status.

Regional assessment found that imposex status was below the BAC in the Irish Sea; elevated above background but below the EAC in the Northern North Sea, Minches and Western Scotland and the Western Channel and Celtic Sea; and above the EAC in the Eastern Channel (Figure 6).

At a UKMS subregion level, 62% of stations in the Greater North Sea and 83% of stations in the Celtic Seas were below the EAC (Figure 4 and Figure 5). When comparing to the UKMS 2018 results, it should be noted that fewer stations are above the EAC in 2024, but this equates to a larger proportion of stations as fewer stations (70) were included in the 2024 assessment compared to 2018 (110 stations).

Figure 6:  The mean VDS (coloured circle) in each biogeographic region relative to the Environmental Assessment Criterion (EAC). A value of 1 occurs when the mean VDS equals the EAC. The horizontal line indicates the upper one-sided 95% confidence limit on the mean. The mean VDS is significantly below the EAC (p < 0.05) if its upper confidence limit is less than 1. Light blue: the mean VDS is significantly below the Background Assessment Criterion (BAC) (p < 0.05). Dark blue: the mean VDS is significantly below the EAC (p < 0.05) but not the BAC. Red: the mean VDS is not significantly below the EAC (p > 0.05).

Trend Assessment

Regional trend assessment showed that imposex was stable in the Eastern Channel and Western Channel & Celtic Sea and a downward trend was observed in the Northern North Sea, Minches & Western Scotland and the Irish Sea (Figure 7). In the Greater North Sea 75% of stations were stable and a significant downward trend was observed at 25% of stations. In the Celtic Seas, 44% of stations were stable and 56% had a significant downward trend.

Figure 7: The trend (circle, triangle) in mean VDS in each UK biogeographic region. The trend is expressed as the odds of exceeding the Environmental Assessment Criterion in one year relative to the previous year. The horizontal line is the associated 95% confidence interval. There is a significant change in mean VDS (p < 0.05) if the confidence interval does not cut the vertical line at 1. Circle: no significant change in mean VDS (p > 0.05). Downward triangle: significant decrease in mean VDS (p < 0.05).

Further information

Individual station assessments

The regional assessment is synthesised from individual assessments from each station (Table 4).

Table 4. Number of individual assessments with each trend and status by biogeographic region and UKMS subregion. Trend assessment; the estimated trend for the Vas Deferens Sequence (VDS, stage of imposex) exceeding the OSPAR Environmental Assessment Criteria (EAC) in one year relative to the previous year in each dog whelk sampling station. Status assessment; the status for imposex relative to EAC at each dog whelk sampling station. Red: VDS not significantly below the EAC, dark blue: VDS significantly below EAC but not significantly below Background Assessment Criteria (BAC); blue: VDS significantly below BAC.

UKMS subregion	Biogeographic region	Trend assessment	Number of stations	Status Assessment	Number of f stations
Greater North Sea	Northern North Sea	upward trend	0	blue	0
Greater North Sea	Northern North Sea	no trend	7	dark blue	7
Greater North Sea	Northern North Sea	downward trend	4	red	4
Greater North Sea	Eastern Channel	upward trend	0	blue	0
Greater North Sea	Eastern Channel	no trend	5	dark blue	3
Greater North Sea	Eastern Channel	downward trend	0	red	2
Greater North Sea	total	upward trend	0	blue	0
Greater North Sea	total	no trend	12	dark blue	10
Greater North Sea	total	downward trend	4	red	6
Celtic Seas	Scottish Continental Shelf	upward trend	0	blue	4
Celtic Seas	Scottish Continental Shelf	no trend	7	dark blue	15
Celtic Seas	Scottish Continental Shelf	downward trend	14	red	2
Celtic Seas	Minches and Western Scotland	upward trend	0	blue	2
Celtic Seas	Minches and Western Scotland	no trend	2	dark blue	0
Celtic Seas	Minches and Western Scotland	downward trend	1	red	1
Celtic Seas	Irish Sea	upward trend	0	blue	12
Celtic Seas	Irish Sea	no trend	7	dark blue	7
Celtic Seas	Irish Sea	downward trend	15	red	3
Celtic Seas	Western Channel and Celtic Sea	upward trend	0	blue	0
Celtic Seas	Western Channel and Celtic Sea	no trend	8	dark blue	5
Celtic Seas	Western Channel and Celtic Sea	downward trend	0	red	3
Celtic Seas	total	upward trend	0	blue	18
Celtic Seas	total	no trend	24	dark blue	27
Celtic Seas	total	downward trend	30	red	9

The majority of individual status assessments (Table 4) were acceptable however there are a still a number of individual stations failing even in areas where the regional assessment has passed overall. Each region has at least one station where the mean VDS is not significantly below the EAC (red).

Also, sites where there were no dog whelks present are not included in the assessment. In the 2017 survey dog whelks were absent at three of the sites: Mallaig Harbour (West Scotland), Sandhaven East (North East Scotland) and Rockliffe (Irish Sea). These sites were selected for sampling because their 2010 assessment result was above the EAC. In 2010, there was a decreasing trend in imposex at Mallaig Harbour, so the site was improving, while there was no trend of improvement at Sandhaven East or Rockliffe. If dog whelk extinction is a result of tributyltin exposure, then this classification cannot be modelled in the assessment of Vas Deferens Sequence Index. There may also be other reasons for the population decline. The Sandhaven East site had a high Vas Deferens Sequence Index score in 2004, 2005, 2007 and 2010, so it is possible that tributyltin exposure has substantially contributed to the local extinction of dog whelks at this site. Although these results cannot be included in the assessment, in the 2022 survey which is out with the time period for this assessment, there were sufficient dog whelk populations at Sandhaven East and Rockliffe to sample for imposex again.

Individual trend results (Table 4) show that no upwards trends were observed at any of the individual stations. All stations are either showing a decreasing trend or stable level of imposex.

Unfortunately, the majority of stations where the imposex status exceeds the EAC are stable indicating that improvements cannot be expected based on the current data. Only one site within Sullom Voe in Shetland in the Scottish Continental Shelf biogeographic region has a decreasing trend, the others are stable.

Imposex in Sullom Voe

The Sullom Voe site is part of a specific monitoring programme in Sullom Voe funded by the Shetland Oil Terminal Environmental Advisory Group (SOTEAG) initiated in 1987. Due to significant inputs of tributyltin prior to the ban on tributyltin anti-foulants, SOTEAG established an intensive regular monitoring programme there. The survey reports are available from SOTEAG (www.soteag.org.uk). The programme now represents the longest consistent data set of biological effects of contaminants on marine organisms in the UK. Since the tributyltin ban was implemented, there has been a consistent improvement in both the Vas Deferens Sequence Index scores across the area and in dog whelk abundance at the most impacted sites (Gubbins and others., 2010). None of the 20 sites had Vas Deferens Sequence Index scores above the EAC in each of the last 2 surveys (Moore and others. 2018, Moore and others. 2022). Only one site there is now considered above EAC following status assessment, and as the level of observed imposex is significantly decreasing there, this suggests that the site is progressing to good status.

Confidence Assessment

Overall, there is high confidence in the quality of the data used for this assessment. The data have been collected over many years using established sampling methodologies. There is sufficient temporal and spatial coverage and no significant data gaps in the areas assessed over the relevant time periods. The synthesis of monitoring site data for the assessment area scale are based on established and internationally recognised protocols for monitoring and assessment per monitoring site, therefore there is also high confidence in the methodology.

Conclusions

Imposex was not at a level that was causing significant harm in four out of the five biogeographic regions assessed. 62% of stations in the Greater North Sea and 83% of stations in the Celtic Seas were below safe environmental limits for imposex. There are still some individual stations where imposex exceeds the EAC. The imposex monitoring programme has reduced since 2010 and now focuses on those sites that are most at risk. This makes comparing data between UKMS assessments difficult. The trend assessment concluded that imposex occurrence in the UK is now stable or decreasing. In summary, the UKMS target for this indicator has largely been met.

The regional assessment, individual station results and the detailed studies at the Sullom Voe oil terminal, indicate a considerable improvement in the reproductive status of dog whelks following the ban on tributyltin-based anti-foulant paints. Dog whelks are still significantly exposed to tributyltin at only a very limited number of sites.

Knowledge gaps

There was insufficient data for a regional assessment in the Scottish Continental Shelf and Southern North Sea biogeographic regions. The number of stations in the Scottish Continental Shelf should be increased to give sufficient geographic spread to enable this. However, the Southern North Sea biogeographic region does not have shorelines to provide dog whelk habitat so there will never be sufficient sites here for assessment.

Dumpton syndrome is a genetic abnormality which has been shown to reduce the sterilising effect of TBT in dog whelks (Quintela and others. 2002). This can potentially interfere with imposex measurements and should be considered in TBT specific effect monitoring programmes. The current protocol (ICES TIMES 24) has limited guidance on Dumpton Syndrome and this should be reviewed.

References

Bailey, S. K., Davies, I. M., 1988. Tributyltin contamination around an oil terminal in Sullom Voe (Shetland). Environ. Pollut. 55, 161–172. Available via: https://doi.org/10.1016/0269-7491(88)90149-2

Gibbs, P.E., P.L. Pascoe, Burt G.R.,1988. Sex Change in the Female Dog-welk Nucella lapillus, Induced by Tributyltin from Antifouling Paints. J. Mar. Biol. Ass. U.K. 68, 715-731. Available via: https://doi.org/10.1017/S0025315400028824

Gubbins, M. J., Moore, J., Fryer, R., & Davies, I. M. (2010, September). Long time series data showing recent recovery of gastropod populations from effects of tri-butyl tin at the Shetland oil terminal. In ICES Annual Science Conference https://www.ices.dk/sites/pub/CM%20Doccuments/CM-2010/F/F0910.pdf

McCullagh, P., Nelder, J.A. 1989. Generalized Linear Models (second edition). Chapman & Hall, London.

Moore, J., Mercer, T. & Anderson, H., 2018. Surveys of dogwhelks Nucella lapillus in the vicinity of Sullom Voe, Shetland, August 2018., Cosheston, Pembrokeshire and Aberdeen: Aquatic Survey & Monitoring Ltd. and Marine Scotland Science. Available at: https://www.soteag.org.uk/files/2019/04/2018-SOTEAG-Dogwhelk-Report.pdf

Moore, J., Campbell, M., Harding, M., Anderson, H. and Bunker, A. (2022). Surveys of dogwhelks Nucella lapillus in the vicinity of Sullom Voe, Shetland, August 2021. A report to SOTEAG from Aquatic Survey & Monitoring Ltd., Cosheston, Pembrokeshire and Marine Scotland Science, Aberdeen. https://www.soteag.org.uk/environmental-monitoring/monitoring-reports/

Nicolaus, M. E. E., Robinson, C. D., and Fryer, F. (2018). Time trend and status for organotin-specific biological effects (imposex in gastropods). UK Marine Online Assessment Tool, available at: https://moat.cefas.co.uk/pressures-from-human-activities/contaminants/imposex/

OSPAR Commission. 2004. List of Chemicals for Priority Action (Revised 2013). OSPAR Agreement 2004-12. Available via: https://www.ospar.org/documents?d=32745

OSPAR Commission. 2008. JAMP Guidelines for Contaminant-Specific Biological Effects (Replaces Agreement 2003-10). OSPAR Agreement 2008-09. Available via: https://www.ospar.org/documents?d=32799

OSPAR Commission. 2010. OSPAR Coordinated Environmental Monitoring Programme (CEMP). OSPAR Agreement 2010-1 (amended in 2011, 2012, 2013). OSPAR Agreement 2010-1. Available via: https://www.ospar.org/documents?v=32943

Parmentier, K. F. V., Verhaegen, Y., De Witte, B.P., Hoffman, S., Delbare, D.H.R., Roose, P.M.,  Hylland, K.D.E, Burgeot, T., Smagghe, G.J. and Cooreman, K. (2019). Tributyltin: A Bottom–Up Regulator of the Crangon crangon Population? Front. Mar. Sci., 15 October 2019. Available via: https://doi.org/10.3389/fmars.2019.00633

Quintela, M., Barreiro, R., Ruiz, J.M. (2002). Dumpton Syndrome reduces the tributyltin (TBT) sterilising effect on Nucella lapillus (L.) by limiting the development of the imposed vas deferens, Marine Environmental Research, 54, 3–5, 657-660.

Smith, B.S. (1981). Tributyltin compounds induce male characteristics on female mud snails Nassarius obsoletus = Ilyanassa obsoleta. J. Appl. Toxicol. 1, 141–144. Available via: https://doi.org/10.1002/jat.2550010302

Uc-Peraza, R.G., Castro, I.G. and Fillmann, G. (2022). An absurd scenario in 2021: Banned TBT-based antifouling products still available on the market. Science of the Total Environment 805: 150377. Available via: https://doi.org/10.1016/j.scitotenv.2021.150377

Waldock MJ, Waite ME, Thain JE (1988) ‘Inputs of TBT to the marine environment from shipping activity in the UK’ Environmental Technology Letters, 9: 999–1010.

Authors

Hannah Anderson¹  

¹Marine Directorate of the Scottish Government

Assessment metadata

Assessment Type	UK Marine Strategy Framework Directive Indicator Assessment
	D8
	D8.2 Effects of Contamination
	Marine Strategy Part One
Point of contact email	marinestrategy@defra.gov.uk
Metadata date	Sunday, June 1, 2025
Title	Organotin-specific biological effects (imposex in gastropods)
Resource abstract
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Conditions applying to access and use	© Crown copyright, licenced under the Open Government Licence (OGL).
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Dataset DOI	The Scottish Government, Marine Directorate. 2025. https://doi.org/10.7489/12541-1

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