Imposex levels in the dogwhelk Nucella lapillus (L.)—continuing improvement at high latitudes

In 1990, restrictions on the use of tributyltin (TBT)-based antifouling paints were implemented in Iceland. A previous study showed that the level of imposex in the dogwhelk, Nucella lapillus, in Icelandic waters had decreased significantly between 1992 and 1998. In this study, we repeated the survey on imposex in N. lapillus at 33 locations from the Icelandic coast in 2003. The results indicated that both Vas Deferens Sequence Index (VDSI) and Relative Penis Size Index (RPSI) had further declined in 13 locations since 1998. Among these 13 sites, RPSI was reduced to zero in five cases. While improvements from 1992/1993 to 1998 were seen in reduced levels of imposex near both large and small harbours, the pattern from 1998 to 2003 was somewhat different, with improvement mainly observed near smaller harbours. No significant changes in imposex levels near larger harbours occurred over this period. Although the imposex levels still remain high near the large harbour complexes in Reykjavík and Hafnarfjörður, it is evident that regulations, including the use of less toxic antifouling paints and community action, have lead to substantial improvements in the marine environment of Iceland. International Maritime Organisation’s ban on the application of TBT after 2003 is apparently necessary to allow further improvements in larger harbours. The environmental effects of new antifoulants replacing TBT need to be further evaluated.     

Metallothioneins and trace metals in the dogwhelk Nucella lapillus (L.) collected from Icelandic coasts

Different sizes of the dogwhelk Nucella lapillus were collected from eight locations along the southwest and north coasts of Iceland. Concentrations of total metallothioneins (MTs) and heavy metals (Cd, Cu, Cr, Mn, Ni, and Zn) were analysed using the silver saturation method and inductively coupled plasma-atomic emission spectrometry. The level of tributyltin (TBT) contamination was also assessed using imposex indices, the vas deferens stage index (VDSI) and relative penis size index (RPSI). Gufunes N. lapillus presented the highest values of VDSI (4.0) and RPSI (11.1), followed by Grenivík individuals (VDSI = 3.0; RPSI = 0.9), while the Strandakirkja population showed the lowest VDSI (0.3) and zero RPSI. At a standardised size (0.25 g dry soft-body weight), Grenivík N. lapillus exhibited significantly higher concentrations of all metals whereas overall metal concentrations were significantly lower in individuals from Strandakirkja and Garðskagi compared to other study sites. Partial correlation analyses with size correction indicated that MT concentrations were better correlated with Cd and Cu concentrations than with other metals. At the standard size, the pattern of MT concentrations in N. lapillus from different sites was, however, very different from those of metal profiles. Such discrepancies between the patterns of MT and metals in N. lapillus might be explained by the fact that MT induction could be influenced by various factors such as temperature, dietary metal intake, growth rate and co-existence of other MT-inducing chemicals.     

Long-term temporal trends (1992-2008) of imposex status associated with organotin contamination in the dogwhelk Nucella lapillus along the Icelandic coast

Using the dogwhelk Nucella lapillus as a biomonitor, we evaluated the organotin contamination along the Icelandic coast over nearly two decades. In 2008, adult dogwhelks collected from 30 locations were examined for imposex status. In 2009, tissue concentrations of six organotin species in dogwhelks from 16 of the 30 locations were analysed using gas chromatography-mass spectrometry. Tributyltin was the most predominant residue ranging from 2.07 to 70.38 μg kg(-1) dw, while triphenyltin was also detected at concentrations up to 22.79 μg kg(-1) dw. Higher total organotin concentrations and imposex indices were observed at locations near large harbours (Reykjavík and Hafnarfj?reur). By comparing the current imposex results with those of previous surveys (1992-2003), we found that recovery was slow near the large harbours, but more apparent near the smaller harbours. We also observed a notable increase in imposex at several northwest sites implying incessant input of organotins.     

Long-term temporal trends (1992–2008) of imposex status associated with organotin contamination in the dogwhelk Nucella lapillus along the Icelandic coast

Using the dogwhelk Nucella lapillus as a biomonitor, we evaluated the organotin contamination along the Icelandic coast over nearly two decades. In 2008, adult dogwhelks collected from 30 locations were examined for imposex status. In 2009, tissue concentrations of six organotin species in dogwhelks from 16 of the 30 locations were analysed using gas chromatography–mass spectrometry. Tributyltin was the most predominant residue ranging from 2.07 to 70.38 μg kg⁻¹ dw, while triphenyltin was also detected at concentrations up to 22.79 μg kg⁻¹ dw. Higher total organotin concentrations and imposex indices were observed at locations near large harbours (Reykjavík and Hafnarfjörður). By comparing the current imposex results with those of previous surveys (1992–2003), we found that recovery was slow near the large harbours, but more apparent near the smaller harbours. We also observed a notable increase in imposex at several northwest sites implying incessant input of organotins.     

Imposex in Morula Granulata as Bioindicator of Tributyltin (TBT) Contamination in the Dampier Archipelago, Western Australia

This study was undertaken to examine the use of imposex in the tropical neogastropod whelk Morula granulata as bioindicator of tributyltin (TBT) contamination. Samples were collected from sites throughout the Dampier Archipelago; both impact sites close to intensive shipping activity and remote control sites. TBT in this area originates mainly from commercial vessels using the Port of Dampier that are >25 m in length and exempt from legislation controlling the use of TBT in antifouling paints. A field survey was undertaken in July 1997; 100 M. granulata were taken at each of 18 sites with varying vessel activity, and examined for imposex. The level of TBT contamination in the Archipelago was low; ranging from <0.3 to 25 ng Sn l⁻¹ in water,<0.3 to 80 ng Sn g−¹ in oyster tissue (Saccostrea cuccullata – prey of M. granulata), and <0.3 to 33 ng Sn g⁻¹ in whelks. Percentage of imposex in M. granulata ranged from 0% to 57%, and was correlated with distance to vessel activity (r=0.646, p<0.05). The only significant relationship of imposex with butyltin concentrations was with TBT in oysters (r=0.826, p<0.05), and dibutyltin (DBT) in whelks (r=0.783, p<0.05). It is postulated that this is because of interspecies variation in ability to metabolize TBT to DBT and MBT (monobutyltin), as well as induction of imposex in earlier life stages, so that imposex in adults could be a reflection of prior contamination. M. granulata is a suitable bioindicator of TBT contamination in the Dampier Archipelago, which could be used throughout the Indo-Pacific given its abundance in the region.     

Integrative assessment of organotin contamination in a southern European estuarine system (Ria de Aveiro, NW Portugal): tracking temporal trends in order to evaluate the effectiveness of the EU ban

Organotin (OT) compounds have been used as biocide agents in antifouling paints since the mid 1960s and are now ubiquitous in the marine environment. Due to their high toxicity to non-target species they were banned from antifouling paints in the European Union in 2003 (2002/62/EC directive). The aim of the present work is to assess any obvious decline of the OT environmental levels at Ria de Aveiro (NW Portugal) after the ban. The organotins - monobutyltin (MBT), dibutyltin (DBT), tributyltin (TBT), monophenyltin (MPT), diphenyltin (DPT), triphenyltin (TPT), monoctyltin (MOT), dioctyltin (DOT) and trioctyltin (TOT) - were quantified in the gastropod Nassarius reticulatus, in the mussel Mytilus galloprovincialis and in sediments. Imposex (imposition of male characters on females of gonochorist gastropods) in N. reticulatus was additionally used as a biomarker of TBT pollution. Time comparisons show a slight decrease of imposex between 2003 and 2005 probably as a consequence of the EU ban, though in some cases this trend seems to have started earlier since 2000. The fraction of TBT relatively to its metabolites has been decreasing over the last years but still remains high suggesting that there are still recent inputs of this compound into the study area.     

Spatial and temporal changes of TBT pollution along the Portuguese coast: inefficacy of the EEC directive 89/677

Nucella lapillus imposex (superimposition of male characters onto prosobranch females) and organotin body burden were surveyed in the Portuguese coast in 1997 and 2000. Time comparisons of the available data on Nucella lapillus imposex in the Portuguese coast indicate a global increase of TBT pollution in recent years, revealing the inefficacy of the 1993 legislation that bans the use of TBT paints on small boats (<25 m). The absence or scarcity of the species inside harbours, which are the most polluted sites in Portugal, is probably a consequence of extinction due to female sterilisation by TBT.     

Organotin compounds in seawater and Mytilus galloprovincialis mussels along the Croatian Adriatic Coast

In this work, data on the level of organotin compounds (OTCs) in seawater and mussels collected along the entire Croatian Adriatic Coast are presented. The samples were collected in 2009 and 2010 at 48 locations representing different levels of maritime activities, including marinas, ports and reference sites. Butyltins (BuTs) were found in all analyzed samples, representing >97% of OTCs, and ranged from 0.46 to 27.98 ng Sn L(-1) in seawater and from <6 to 1675 ng Sn g(-1) in mussels. The results indicate a recent input of TBT, with the highest concentrations of BuTs found in the marinas. It appears that the Adriatic coast is still polluted with TBT despite the fact that TBT-containing antifouling paints have been banned in Croatia since 2008. It is questionable how much TBT pollution decreased since 2005, when a high incidence of imposex was established in the same area.     

Imposex in Thais gradata and Chicoreus capucinus (Mollusca, Neogastropoda, Muricidae) from the Straits of Johor: A Case Study using Penis Length, Area and Weight as Measures of Imposex Severity

Imposex, or the presence of a pseudopenis in female snails, is quantified by comparing the length of the female pseudopenis with the male penis. However, many muricid gastropods in the Malayan archipelago possess penes that are flagellate and coiled, making linear measurement difficult under the microscope. In addition, it is unclear if penis length is dependent on shell size. Accurate assessment of penis size is a necessary step towards determining the severity of imposex (and implicitly, the amount of organotins from antifouling paints that is associated with this phenomenon). Two mangrove muricid gastropod species, Thais gradata and Chicoreus capucinus, were collected from six sites along the Johor Straits. Penis/pseudopenis length and area measurements based on digitalized camera lucida drawings were generally well correlated with penis/pseudopenis dry weight, although penis area appeared to be a marginally better variable than penis length for T. gradata. Penis dry weight was also well correlated with shell height in male T. gradata, while no significant correlation was detected for female T. gradata, suggesting pseudopenis size alone may be a better measure of imposex than the relative penis size index (RPSI) for this species. There was no obvious relationship between penis size and shell height for either sex in C. capucinus.     

Magnetic characteristics of sediment grains concurrently contaminated with TBT and metals near a shipyard in Busan,Korea

Bottom sediments near shipyards are often susceptible to receiving accidental spills of TBT and metals or their degradation products from hull scraping of antifouling system paints applied prior to 2008, when the AFS Convention 2001 was not in force. We investigated TBT and metal contamination of sediments near the shipyards of a small marina located in Busan, Korea and found that they were highly contaminated with TBT, Cu, and Zn. To better understand the environmental impacts and to make an optimal remediation plan, we characterized individual antifouling fragments in terms of metal and TBT contents, magnetic properties, and grain-size. Coarse-sized individual antifouling fragments exhibited simultaneously high levels of TBT, metals and high magnetic susceptibility, and appeared to be a major source of pollution in the sediment. Therefore, magnetic separation in combination with size-separation appears to be a cost-effective remediation method to remove the TBT and metals from contaminated shipyard sediments.     

Seasonal changes in imposex and tissue burden of butyltin compounds in Thais clavigera populations along the coastal area of Mirs Bay, China

We assessed the current status of tributyltin (TBT) contamination of Thais clavigera (Gastropoda) along the coastal area of Mirs Bay, China for the first time. The snail samples were collected from 10 different sites in the summer (June) and winter (December) of 2006, respectively. They were analyzed for imposex status, i.e. relative penis size index (RPSI) and vas deferens sequence index (VDSI), followed by quantification of butyltins in their tissues. Most of the collected females suffered from imposex, but the level of butyltin contamination varied with the distance from Yantian Port, which is currently the fourth busiest container port in the world. The tissue concentration of TBT varied with season. For a particular site, the winter samples in general contained much higher concentration of TBT than the summer samples. RPSI, VDSI and organotin concentrations were higher in T. clavigera collected from sites closer to the Port, such as the Seafood Street and Kat O. Both RPSI and VDSI were positively correlated with the tissue burden of tributyltin. VDSI exhibited little seasonal variability, whereas RPSI showed marked seasonal variability, with lower values in the summer samples. The current results will serve as an important reference for long-term monitoring of butyltin contamination in this area.     

Seasonal changes in imposex and tissue burden of butyltin compounds in Thais clavigera populations along the coastal area of Mirs Bay, China

We assessed the current status of tributyltin (TBT) contamination of Thais clavigera (Gastropoda) along the coastal area of Mirs Bay, China for the first time. The snail samples were collected from 10 different sites in the summer (June) and winter (December) of 2006, respectively. They were analyzed for imposex status, i.e. relative penis size index (RPSI) and vas deferens sequence index (VDSI), followed by quantification of butyltins in their tissues. Most of the collected females suffered from imposex, but the level of butyltin contamination varied with the distance from Yantian Port, which is currently the fourth busiest container port in the world. The tissue concentration of TBT varied with season. For a particular site, the winter samples in general contained much higher concentration of TBT than the summer samples. RPSI, VDSI and organotin concentrations were higher in T. clavigera collected from sites closer to the Port, such as the Seafood Street and Kat O. Both RPSI and VDSI were positively correlated with the tissue burden of tributyltin. VDSI exhibited little seasonal variability, whereas RPSI showed marked seasonal variability, with lower values in the summer samples. The current results will serve as an important reference for long-term monitoring of butyltin contamination in this area.     

Occurrence and effects of organotins on adult common whelk (Buccinum undatum) (Mollusca, Gastropoda) in harbours and in a simulated dredging situation.

Transplanted common whelk (Buccinum undatum) (Mollusca, Gastropoda) accumulated fairly high levels of organotins (tributyltin (TBT) and triphenyltin (TPT)) during exposure in three harbours with different TBT contamination. This did not though lead to an increase in imposex frequency in the adult females studied. Simulating harbour dredging in an experiment using suspended sediment from one of the harbours only resulted in a low concentration of TBT in the tissues of the common whelk and subsequently no changes in the occurrence and degree of imposex. The common whelk seemed to receive the main part of TBT from the water column and the limited bioaccumulation in the experiment indicates that desorption of TBT from the suspended sediment was slow. After TBT has been totally banned, dredging of contaminated sediments will cause increased exposure of the biota to TBT. Due to slow desorption the increase may however, be slight and temporary to pelagic and epibenthic species unless the settled particles are resuspended.     

Seasonal changes in imposex and tissue burden of butyltin compounds in Thais clavigera populations along the coastal area of Mirs Bay,China

We assessed the current status of tributyltin (TBT) contamination of Thais clavigera (Gastropoda) along the coastal area of Mirs Bay, China for the first time. The snail samples were collected from 10 different sites in the summer (June) and winter (December) of 2006, respectively. They were analyzed for imposex status, i.e. relative penis size index (RPSI) and vas deferens sequence index (VDSI), followed by quantification of butyltins in their tissues. Most of the collected females suffered from imposex, but the level of butyltin contamination varied with the distance from Yantian Port, which is currently the fourth busiest container port in the world. The tissue concentration of TBT varied with season. For a particular site, the winter samples in general contained much higher concentration of TBT than the summer samples. RPSI, VDSI and organotin concentrations were higher in T. clavigera collected from sites closer to the Port, such as the Seafood Street and Kat O. Both RPSI and VDSI were positively correlated with the tissue burden of tributyltin. VDSI exhibited little seasonal variability, whereas RPSI showed marked seasonal variability, with lower values in the summer samples. The current results will serve as an important reference for long-term monitoring of butyltin contamination in this area.     

Butyltin compounds,sterility and imposex assessment in Nassarius reticulatus (Linnaeus, 1758), prior to the 2008 European ban on TBT antifouling paints,within Basque ports and along coastal areas

Levels of imposex (superimposition of male characters, upon females) and the presence of sterile females are assessed in the gastropod Nassarius reticulatus (L.), at 35 locations in the Basque Country. At 18 of these localities, organotin bioaccumulation (tributyltin (TBT); dibutyltin; monobutyltin) was evaluated, using isotope dilution GC–ICP–MS. Higher imposex levels and TBT body burden were found in confined harbours, with large vessel traffic or the presence of an offshore fleet. The highest values were found for the port of Pasaia, near to a shipyard (a relative penis size index of up to 92%, and TBT body burden up to 405 ng g^?1 – given on a dry weight basis as Sn). Imposex effects were evaluated also in parasitized females, at some of the sampling sites. The percentage of presence of c-type Vas Deferens sequence stages (i.e., with vas deferens beginning at the oviduct opening) was higher in parasitized females. In turn, there was an absence of highly convoluted oviduct in parasitized females.     

Imposex in the indigenous Nassarius kraussianus (Mollusca: Neogastropoda) from South African harbours

Nassarius kraussianus populations in the Durban and Richards Bay harbours (along the eastern seaboard of southern Africa) and in the Knysna lagoon (southern Cape coast) showed imposex development, confirming bioavailability of tributyltin (TBT) in these waterways. Incidence of imposex (which ranged from 29% to 100%) and relative penis length of females (RPL; which ranged from 1.3% to 55.2%) were markedly variable among populations from different sites in each waterway, indicative of localised effects of TBT contamination. Shell length of the snails was apparently not correlated with contamination level, as assessed from imposex measurements. While population imposex features are easy to determine and often provide a sensitive biomarker of TBT exposure, the discussion outlines reservations when extrapolating these to general ecological situations. Additionally, this study represents the first published report on the topic for sub-Saharan, African harbours, some of which seem remarkably less affected than suggested for other world regions.     

Organotins (TBT and DBT) in water, sediments, and gastropods of the southern Venice lagoon (Italy)

The release of tributyltin (TBT) from maritime traffic represents one of the main problems of direct, diffuse, and continued contamination of the marine environment. In the present survey, the concentrations of TBT and dibultytin (DBT) in brackish waters, sediments, and the gastropods Nassarius nitidus were evaluated in order to estimate the contamination of the southern part of the Venice lagoon. TBT and DBT were determined by GC-MS/MS. Recent contamination of TBT was found in brackish waters near marinas, whereas the highest concentrations of TBT and DBT were observed in surface sediments at dockyards and harbours. High content of organotin in the gastropods sampled near the dockyards, harbours, and marinas showed a mobilisation from the sediments through the food web. The present study allowed assessment of whether, despite the ban on the use of TBT paints, waters, sediments, and biota were still being contaminated by organotin compounds in the southern Venice lagoon.     

A review and assessment of tributyltin contamination in the North Sea,based on surveys of butyltin tissue burdens and imposex/intersex in four species of neogastropods

It is evident from measures of butyltin tissue burdens and imposex or intersex in neogastropods that tributyltin (TBT) contamination of coastal waters and open parts of the North Sea is now low. It has been declining for at least the past decade. This is probably due to two measures. First, regulations prohibiting the use of TBT-based paints on small boats and fish farms have reduced inputs of TBT from these sources so that they are now negligible (except possibly where the regulations are flaunted). Second, there is evidence from sites, where commercial vessels are the sole source of TBT, that the adoption of TBT SPC paints has been effective in reducing environmental levels of these contaminants. However, poor dockyard practices, allowing TBT-contaminated wastes, including paint flakes, to accumulate in sediments have left a legacy of hot-spots of contamination in some ports. The impact is localised so that TBT contamination is low in coastal areas immediately adjacent to ports.     

The significance of imposex levels and TBT contamination in the red whelk, Neptunea antiqua (L.) from the offshore Irish Sea

The extent to which open seas and oceanic waters have been contaminated by TBT is unclear since most sampling programmes have concentrated on inshore areas, particularly near harbours. Accordingly, the red whelk, Neptunea antiqua L. (Mollusca: Prosobranchia), a sublittoral and dioecious prosobranch species, was selected to investigate the potential effects of TBT-induced imposex in the central western Irish Sea. The presence of imposex was noted in > 90% of all female whelks that were examined on a monthly basis over a 12-month period. However, the proliferation of the vas deferens was not considered severe enough to affect the reproductive capabilities of the population. Low concentrations of butyltins were detected in the soft tissues of all whelks examined, ranging from 0.009 to 0.112 microg g(-1) Sn dry wt There was no significant correlation between the documented imposex stages and total butyltin contamination, indicating that the species is not a reliable bioindicator species of the effects of this contaminant.     

Incidence of imposex in thais orbita from Port Phillip Bay (Victoria, Australia), following 10 years of regulation on use of TBT.

Imposex, the phenomenon in which induced male sex characteristics are superimposed on normal females, still occurs widely in the gastropod Thais orbita from Port Philip Bay, and its incidence is greatest in areas that have high boating and shipping activities. Compared to 1992, both the extent and severity of imposex has reduced. By inference, this means that pollution by tributyltin (TBT) in Port Phillip Bay has decreased and that the bans limiting its use to vessels greater than 25 m in length, in place since 1989, have been effective. However, TBT pollution is still an issue at locations that are adjacent to major ports, such as the Port of Melbourne, where TBT from large ships and ship maintenance activities continues to pollute fish habitats. It is anticipated that the incidence of imposex, and therefore TBT pollution, will continue to decrease in Port Phillip Bay as long as the bans currently in place continue to be observed. If the trends observed in the present study continue, then it is unlikely, with the notable exception of commercial ports, that TBT will pose a threat to the health of fish habitats in Port Phillip Bay.