Status and Trends in the Levels of Imposex in Marine Gastropods (TBT in Shellfish)

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 et al., 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 oil terminals 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 also 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 et al., 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. As there are still countries where TBT is not banned, TBT is still manufactured in the USA and is available on the market (Uc-Peraza, 2022).

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.

In assessing data generated through the Coordinated Environmental Monitoring Programme (CEMP), OSPAR states that the primary assessment value used in the assessment of contaminant concentrations in sediment and biota “corresponds to the achievement, or failure to achieve, statutory targets or policy objectives for contaminants in these matrices” (OSPAR, 2009b). These assessment criteria were specifically compiled for the assessment of CEMP data on hazardous substances contributing to the QSR 2010 (OSPAR, 2009a,c). Their use was considered an interim solution for the purposes of the QSR 2010 and were to be used until more appropriate assessment methodology could be agreed upon and implemented. These ‘interim’ criteria have also been used in the annual CEMP assessments since 2010, and will continue to be used until OSPAR agrees on the adoption of improved assessment criteria and subject to the conditions set out in the agreement.

OSPAR 2017 Intermediate Assessment (IA) values are not to be considered as equivalent to proposed European Union Marine Strategy Framework Directive (MSFD) criteria threshold values. However, they can be used for the purposes of their MSFD obligations by those Contracting Parties that wish to do so.

Provenance and limitations of BACs

Background assessment concentrations (BACs) have been developed by OSPAR to test whether measured concentrations are near background levels for naturally occurring substances and close to zero for man-made substances, the ultimate aim of the OSPAR Hazardous Substances Strategy 2010-2020. Mean concentrations significantly below the BAC are said to be ‘near background’ (for naturally occurring concentrations). BACs are statistical tools defined in relation to the background concentrations or low concentrations, which enable statistical testing of whether measured concentrations could be considered to be near background levels.

Background concentrations (BC) are assessment tools intended to represent the concentrations of certain hazardous substances that would be expected in the North-East Atlantic if certain industrial developments had not happened. They represent the concentrations of those substances at ‘remote’ sites, or in ‘pristine’ conditions based on contemporary or historical data respectively, in the absence of significant mineralisation and/or oceanographic influences. In this way, they relate to the background values referred to in the OSPAR Hazardous Substances Strategy 2010-2020. BCs for artificial substances should be regarded as zero. It is recognised that natural processes such as geological variability or upwelling of oceanic waters near the coast may lead to significant variations in background concentrations of contaminants, for example trace metals. The natural variability of background concentrations should be taken into account in the interpretation of CEMP data, and local conditions should be taken into account when assessing the significance of any exceedance.

Low concentrations (LC) are values used to assist the derivation of BACs where there have been difficulties in assembling a dataset on concentrations in remote or pristine areas from which to derive background concentrations. LCs were prepared on the basis of datasets from areas that could generally be considered remote, but which could not be guaranteed to be free from influence from long-range atmospheric transport of contaminants. LCs have also been used to assess concentrations in sediments from Spain due to the specific bulk composition of sediments from the coasts of the Iberian Peninsula. It is recognised that natural background concentrations may be lower than LCs and that they may not be directly applicable across the entire OSPAR Maritime Area.
For imposex, BACs are based on the formerly used imposex classes.

Provenance and limitations of EAC

Environmental assessment criteria (EAC) were developed by OSPAR and ICES for assessing the ecological significance of sediment and biota concentrations. Some EACs were specifically compiled for assessing CEMP data on hazardous substances contributing to the QSR 2010 (OSPAR 2009c). The EACs do not represent target values or legal standards under the OSPAR Convention and should not be used as such. The EACs were set such that hazardous substance concentrations in sediment and biota below the EAC should not cause chronic effects in sensitive marine species, nor should concentrations present an unacceptable risk to the environment and its living resources. EAC continue to be developed by OSPAR for use in data assessments.

Countries submit imposex monitoring data to ICES DOME . The imposex assessment presented here was based on data from the ICES database from 1993 to 2020 (with the exception of Portugal, where a separately submitted dataset was used).

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 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, 2008a) 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). Two time series of Ocenebra erinaceus (European sting winkle) were included in the trend assessment, but not in the status assessments (due to the absence of BACs or EACs). The great majority of monitoring stations are of either Nucella lapillus (dog whelk) or Tritia reticulata (Table a). Periodically (typically every 1-4 years), the degree of imposex is measured using the Vas Deferens Sequence (VDS, described below) for a number of snails in each station, which forms the basis for assessment of status and temporal trends (Table a). The VDS index (average VDS) is shown for all stations in OSPAR's contaminants assessment tool OHAT ( https://dome.ices.dk/ohat/?assessmentperiod=2022 ).

In addition, a related sexual development syndrome, intersex, is monitored in Littorina littorea (common periwinkle) in seven Danish, Dutch, and German stations on the Wadden Sea coast. No status assessment criteria have been developed for intersex, so only trends are monitored on these stations.

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 b). VDS = 0 indicates normal genitals, VDS = 5, and VDS = 6 indicates that the female is incapable of reproducing.

Imposex status

Two assessment criteria are used to assess the status of imposex in snails: BACs and EAC.

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. Both criteria are available for Nucella lapillus and Neptunea antiqua, while only EAC is available for Tritia reticulata and Buccinum undatum (Table c).

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 OSPAR regional level).

Time series of imposex measurements are assessed for status against the EAC if: there are at least three years of data, and there is at least one year with data in the period 2015-2020.

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: OSPAR contaminants assessment area
• Random model: status estimation variation + residual variation.

Imposex temporal trends

The ICES database contains a mixture of time series, some with individual measurements only, some with pooled measurements (i.e., data on several individuals combined into one number), and some with a mixture of individual and pooled measurements. In all cases, fitting a temporal trend requires that there was data for at least one year in the period 2015 to 2020 (with the exception of a few Portuguese times series, which were treated as a special case).

For the time series containing individual measurements only, the trend in each 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).

For the time series containing pooled measurements only, a linear trend line was fitted if there were at least four years of data. The trend was then transformed to make comparison among series possible.

For time series that contained a mixture of individual and pooled measurements, the time series was truncated to use the individual-measurement method if there were enough data (i.e., three years); otherwise, a linear trend was fitted.
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 OSPAR contaminants assessment area. 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.

General guidelines for assessment in CEMP

Methods for data screening, treatment of quality assurance information, temporal trend assessment and assessment against criteria used previously by CEMP are described in the CEMP Assessment Manual (OSPAR, 2008b) and in the help files for the contaminants online assessment tool.

Criteria used to assess environmental concentrations of hazardous substances are set out in the OSPAR agreement on CEMP Assessment Criteria for the QSR 2010 (OSPAR, 2009c). The derivation of these criteria for hazardous substances is discussed in a Background Document on CEMP Assessment Criteria for the QSR 2010 (OSPAR, 2009b, 2011). These criteria reflect a two-stage process in which data are compared to concentrations yielding limited risk of biological effects (EAC), and then against BCs or zero, expressed as BACs. The latter reflects the OSPAR Hazardous Substances Strategy 2010-2020, in that concentrations should be at or close to background levels for naturally occurring substances (and zero for man-made substances).

Location of monitoring sites

Imposex is currently monitored at more than 200 sites (Table d and Figure 4) on up to three marine gastropod species.

⁽¹⁾The number of stations was considered to be low for regional assessment

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.

Methodological improvements

The regional assessment for the QSR 2010 was carried out by means of a simple tabulation of the trend and status at each monitoring site.

For the IA 2017 and the QSR 2023, 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.

In the QSR 2010, imposex levels were still substantially higher than at present, although the large majority of imposex time series showed a decreasing trend in the period 1997 to 2008. This indicates that TBT levels in the environment were still high after TBT and other organotins had been in widespread use since the 1960s. While imposex was linked with TBT already in 1981, a general ban on all vessels and offshore installations was not put in place until 2008. Thus, in 2008, as much as 81% of sites still had imposex levels classified as over EAC , in other words outside safe environmental limits (Figure a and Table e).

In 2020, the percentage of sites classified as over EAC has decreased to 22%. 56% of the sites are below safe environmental limits but still above background levels. The remaining 22% of the stations are below BAC , i.e., close to background levels of imposex; this percentage was only 0,5% in 2008 (Table e). A meta-analysis of imposex levels by subregion shows that all subregions can be classified as below safe environmental limits, with the exception of subregions Skagerrak and Kattegat and Iberian Sea. It should be mentioned that these two areas are also the areas with highest proportion of stations with the species Tritia reticulata, which may affect the status assessment (see Methods).

The decline in imposex since 2009 can be seen in all the main OSPAR Regions with enough data, i.e., Region II-IV (Table f). For Region I, there are not enough stations to conclude that there has been an improvement. Region IV, which had the highest percentage of stations over EAC in 2009 (95,5%), still has the highest percentage of stations over EAC (41,1%).

On the subregion level, only two subregions, Skagerrak and Kattegat and the Iberian Sea, are classified as above EAC (Figure a). Of the remaining subregions, four are classified as above BAC but below EAC, while three subregions are classified as below BAC. For the remaining subregions there are not enough data to warrant a metanalysis.

Of the nine OSPAR subregions with enough data, imposex levels have decreased significantly in all subregions (Figure b). The decrease appears to have been highest on the Scottish and Irish West Coast and the Celtic Sea, and lowest in Skagerrak and Kattegat and the Iberian Sea.

The ratio of VDS to EAC showed a large spread within two subregions, Iberian Sea and the Skagerrak and Kattegat. An important cause for this spread appears to be that some sites monitor Nucella lapillus (EAC = 2), while others monitor Tritia reticulata (EAC = 0,3), with the higher (poorer) estimates of status being those for Tritia reticulata (i.e., with the lower EAC). In principle, this should not matter as the different EAC thresholds for each species should compensate for the differences in sensitivity among species. For instance, reasons for the high sensitivity of Nucella lapillus may be that it is predatory and thereby affected by bioconcentration through the food chain, and also it occupies the rocky shore where it is highly exposed to the contaminant micro-layer. However, within each region, it is striking that the VDS/EAC ratio tends to be much higher for Tritia reticulata and Neptunea antiqua than for Nucella lapillus (Figure c). This may be interpreted as an indication that the difference in EAC thresholds may overcompensate for the differences in sensitivity among species. However, this interpretation may be an oversimplification due to inherent differences between the two species. First, the two species occupy different sites: Nucella lapillus is mostly found on the open coast, while Tritia reticulata is found in more sheltered sites, including near harbours, which often are hotspots for TBT. Secondly, they occupy different habitats: Nucella lapillus lives on rocky shores, while Tritia reticulata lives within the sediment. In a TBT-declining situation, the decrease in TBT concentration in the water column can be expected to be faster than its decrease in sediments, since the sediment acts as a sink for TBT. In line with this, Laranjeiro et al., (2018) observed that VDSI levels in N. lapillus start to decrease before Tritia reticulata on the Portuguese coast. Thus, the "correct" difference in EAC thresholds between the species may be different in the declining phase of the TBT problem. This issue has not been further addressed.

Thus, the differences among Regions should be treated with some care, as they may differ in the species used, as well as the exact choice of sample locations within each country. For instance, the high relative VDS values for the Skagerrak and Kattegat and Iberian Sea may be to some extent linked to the low fraction of Nucella lapillus in these two subregions. In most subregions, most or all stations monitor Nucella lapillus, which is more sensitive to TBT than other species used, but in Skagerrak and Kattegat and Iberian Sea, less than 40% of the stations are Nucella lapillus stations.

While the deliterious effects of  TBT became known around 1980, it was not until 2008 (i.e. approximately 30 years later) that TBT became illegal to use in the large majority of coastal nations (and some countries still have not ratified the ban). The ban has clearly had a large effect, as shown by a big decrease in imposex since the QSR 2010. Also, many positive recoveries of local gastropod populations that were formerly decimated by sterility due to imposex, have been documented.

However, although the big picture is a positive one, one should still remember the following:

• Two subregions (Skagerrak and Kattegat, and the Iberian Sea) are classified as being generally above the EAC, i.e., outside safe environmental limits
• Overall, about three quarters of the sampling sites still have a higher than normal frequency of imposex
• While the general coastal environment may be of good status, local hotspots with high TBT concentrations remain. For instance, while routinely monitored stations may have no or very few snails with signs of imposex (Figure a), there still exist hotspots with high TBT concentrations in the marine sediment, typically close to shipyards and busy harbours (reviewed by Beyer et al. 2022).
• The combined effect of TBT and other contaminants on higher trophic levels (e.g., marine mammals) is poorly studied

Given that similar decreasing levels and downward trends are being observed for imposex in different regions, including Ireland, Iceland, Norway and Portugal (Wilson et al. 2015; Guðmundsdóttir et al. 2011; Schøyen et al. 2019), it is clear that legislative prohibitions on the phase out of TBT have been effective and can make a difference to the impact on organisms. While there is general consensus of improvement of environmental status (and the potential for reduced monitoring effort), some “hotspot” or locations may still have imposex levels that are not decreasing or that still exceed EAC thresholds (Beyer et al. 2022). The possible ecological impacts in biota have been investigated only to a limited degree. It is suggested that monitoring efforts could primarily focus on such locations as part of wider spatial and investigative studies (e.g. incorporating other matrices).

The usage of several species for monitoring represents a confounding factor that is difficult to deal with, and it is uncertain whether the present species-specific assessment criteria (EACs) result in an index of TBT contamination that is homogenous across species (Figure d). Literature additionally suggests the potential for a confounding factor in imposex measurements that should be considered in TBT specific effect monitoring programmes, i.e. Dumptons syndrome, which has been shown to reduce the sterilising effect of TBT in dogwhelks (Quintela et al. 2002). Additionally, a strong case has been made that the retinoid X receptor (RXR) and its natural ligand, 9-cis-retinoic acid, play major roles in the development of imposex caused by organotin compounds, but there is still a major question as to why only one group of mollusks and not other invertebrates are affected (Sumpter and Johnson, 2005). In addition research towards the potential for other (or synergistic) contaminants potential to induce the imposition of male characteristics on female gastropods merits inclusion in future research in this area.

Tributyltin has been shown to have significant effects on the fitness of organisms other than mollusks, including shrimp (Parmentier et al., 2019) and sea mammals (Zhang et al., 2022 and references therein). The extent to which non-mollusk species are affected by legacy and ongoing TBT contamination is poorly known. Also, the combined toxicity effects of TBT in combination with other inorganic/organic pollutants is poorly known.

In European waters, TBT has almost universally been replaced by paints containing other tin substances and/or copper, typically in self-polishing paints that slowly release these toxic metals into the environment. Several studies have indicated that such paints increase the concentrations of dissolved or nano-sized particles of these metals (Adeleye et al. 2016 and references therein). Lagerström et al. (2020) show that the use of antifouling paints leads to exceedance of both EQS and PNEC values, and argue that current risk assessment procedures may mean that the environmental risks are underestimated as they fail to take into account that changes in the speciation of dissolved Cu and Zn may increase the proportion of metals that may be considered bioavailable. Thus, there may be good reasons to further investigate whether the current use of TBT substitutes are ecologically sustainable.

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