Spatio-temporal comparisons of imposex status and tissue organotin concentration in the whelk Reishia clavigera collected along the coasts of Dapeng Bay and Daya Bay,Shenzhen, China

Organotin compounds (OTs) have caused widespread adverse effects on marine organisms. As no local restrictions on OT-based antifouling paints have been implemented in China, high concentrations of OTs still occur in coastal environments. In this study, we measured the imposex status and tissue concentrations of OTs in the whelk Reishia clavigera collected along the coast of Dapeng Bay and Daya Bay of Shenzhen, China in 2013. Our results showed that all female whelks suffered from the onset of imposex. The highest concentration of total OTs was 27,756 μg kg⁻¹ dry weight in the samples collected from Shuitousha. Triphenyltin was the most predominant residue, accounting for more than 97.8% of total OTs across all sites. Compared with the results from previous studies, the marine environment of this region is still heavily contaminated with OTs. Therefore, a tightened control is necessary to regulate the use and release of OTs in China.     

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.     

Imposex in Three Marine Gastropod Species in Chile and Potential Impact on Muriciculture

A survey of imposex was conducted between the Bay of San Vicente, Concepción, Chile (36° 50′) and the Bay of Renocavi, Puerto Montt, Chile (41° 35′), to determine if imposex is occurring in an area of collection and cultivation of the gastropod, Chorus giganteus. Imposex was recorded in three chilean muricids C. giganteus, Xanthochorus cassidiformis and Nucella crassilabrum complex. Percentage of imposex in females sampled ranged from 0% to 100%. The degree of expression of imposex was not so severe as to elicit sterility in the individuals surveyed. Incidence of imposex was as high as 47% in areas of harvest of C. giganteus for reproductive and cultivation studies for commercial production of this species. A six percent incidence of imposex was observed in Nucella proximal to the facility for cultivation of C. giganteus. Gastropods of the genus Nucella are used in other countries to monitor incidence of imposex and have demonstrated sensitivity toward tributyltin (TBT), the associated causal agent. Since sex of individuals in muriciculture is determined by the presence or absence of a penis, imposex may lead to erroneous classification of males and females. The incidence and severity of imposex in C. giganteus and related species may have a negative impact on sustainable cultivation and harvest of gastropods in Chile.     

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.     

Biomonitoring of TBT contamination and imposex incidence along 4700 km of Argentinean shoreline (SW Atlantic: From 38S to 54S)

The imposex incidence and TBT pollution were investigated along 4,700 km of Argentinean coast, including city harbors and proximal zones without marine traffic. We analyzed 1805 individuals from 12 gastropod species, including families Volutidae, Muricidae, Nassariidea, Calyptraidae, Marginellidae, and Buccinidae, and found the imposex phenomenon for the first time in six species. In high marine traffic zones, TBT pollution was registered and the percentage of imposex was high, while these occurrences were null in areas without boat traffic. The species that best reflect the degree of imposex were those inhabiting sandy/muddy or mixed bottoms. TBT determination and imposex incidence indicate that pollution was focused only in ports with high marine traffic or in areas where ship hulls are painted. This is the first report of an imposex-sediment approach to evaluate organotin contamination along the coast of a South American country.     

TBT-pollution in the Gulf of Thailand: A re-inspection of imposex incidence after 10 years

Imposex in neogastropods was used to determine the relative TBT distribution in the Gulf of Thailand in 2006. To identify the imposex prevalence, 8757 specimens, belonging to 22 species from five families of neogastropods, were collected at 56 sites in 13 sample areas. These areas were located between the Bight of Bangkok in the north and the Malaysian border in the south. A contamination model was developed to compensate for differences in TBT sensitivity among species and to make comparisons among areas. At every area imposex was found in neogastropods. The highest incidence was in the east side of the Bight of Bangkok off Si Racha and Pattaya and in the southern part around Pattani. The same areas showed the highest frequency of imposex in 1996. While the frequency of imposex appeared to have slightly decreased in these areas, increases were found elsewhere. In Pattani Province this could be related to dumping of highly polluted harbour sediments in the shallow coastal area. The overall frequency of imposex in the Gulf of Thailand significantly increased from 1996 to 2006.     

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.     

A survey of imposex in muricids from 1996 to 2000 and identification of optimal indicators of tributyltin contamination along the east coast of Phuket Island,Thailand

The present investigation is the most extensive survey of imposex in gastropods from the west coast of Thailand. Imposex in Thais distinguenda increased significantly (p < 0.001; Chi Square test for trend) from 1996 to 2000 at 21 stations in Phangna Bay, Thailand. Females with imposex increased, extending from 3.5 km in 1996 to 10 km from the harbour areas in 1999 and 2000. Increasing intensity of imposex was also observed for Thais bitubercularis from 1996 to 2000. The less sensitive species: Morula musiva, Morula granulata, Morula margariticola and Thais rufotincta only developed imposex at the three main areas of intense shipping activities. T. bitubercularis and T. distinguenda are recommended as indicators of tributyltin (TBT) in Southeast Asia because of their sensitivity and wide distribution in the region. The results suggest that TBT contamination is worsening, against global trends, because regulations prohibiting the use of TBT-based paints, do not exist in Thailand.     

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.     

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.     

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.     

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.     

Responses of mud snails from low and high imposex sites to sex pheromones

Imposex, male secondary sexual characteristics in female snails, is a morphological indicator of sub-lethal exposure to organotin compounds. The relation between imposex and behavioral responses to sex pheromones was studied. Responses of snails to sex specific pheromones were determined in laboratory assays. Females and males from a low imposex site and females, imposex females and males from a high imposex site were tested. The snails from the low imposex site showed the expected strong behavioral dimorphism with females responding to male pheromone and males responding to female pheromone. In assays using snails from the high imposex site, female and imposex females showed no dimorphism in response to pheromones and males showed a relatively weak dimorphism. As there was no breeding or egg capsule deposition at the high imposex site, we conclude that even the morphologically normal snails were behaviorally and reproductively compromised.     

Imposex in Japanese gastropods (neogastropoda and mesogastropoda): Effects of tributyltin and triphenyltin from antifouling paints

In Japan, marine pollution by organotin compounds is serious and imposex is known to occur in marine gastropods. However, a detailed survey on imposex had not previously been conducted. The first country-wide survey and laboratory experiments on imposex in Japanese gastropods has now been carried out, and the results are reported herein.     

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.     

Inshore/offshore gradients of imposex and organotin contamination in Nassarius reticulatus (L.) along the Portuguese coast

Imposex and organotin (OT) tissue contamination of the netted whelk Nassarius reticulatus (L.) were assessed in the continental shelves around the main estuaries of the central coast of Portugal (Lisbon: Tagus estuary; Setúbal: Sado estuary) and the main coastal lagoon in the Southern of Portugal (Faro: Ria Formosa). Pollution levels were higher in areas of more intense boat traffic and shipyard activities and imposex showed a clear decreasing gradient from the estuaries to the offshore, in relation to a similar gradient of tissue contamination by tributyltin. Remarkably, imposex was extensively spread over the adjacent continental shelves of Tagus and Sado estuaries. The current work shows that TBT pollution is undoubtedly a matter of concern not only for the above estuaries where harbours are implanted but also for the adjacent continental shelves, regardless the massive dilution of contaminants that may occur in these deeper areas.     

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.     

Assessing the spatial variability,level and source of organic chemical contaminants in bivalve fishing grounds on the Galician coast (NW Spain)

Polychlorinated biphenyls, organochlorine pesticides, organotin compounds and triazines were quantified in sediments and bivalves collected in four areas on the Galician coast. One or several species were analysed at each site depending on their availability, including mussels (Mytilus galloprovincialis), cockles (Cerastoderma edule), clams (Venerupis pullastra and Ruditapes decussatus) and razor shells (Ensis siliqua). The general spatial distribution of contaminants was consistent in spite of the different sources of contamination. High inter-species variability was also observed. M. galloprovincialis and V. pullastra showed the highest levels of contaminants and intra-spatial variability, which highlights them as suitable species to be used as sentinel organisms. The area of O Burgo showed some worrisome results: PCB sediment concentrations were within the range that could cause biological effects. Also the level of heptachlor observed in V. pullastra was above limits accepted on edible seafood. Finally TBT concentration in mussels correlated with concentrations causing imposex in snails.     

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.     

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.