This review provides insights into the distribution and impact of oestrogens and xeno-oestrogens in the aquatic environment and highlights some significant knowledge gaps in our understanding of endocrine disrupting chemicals. Key areas of uncertainty in the assessment of risk include the role of estuarine sediments in mediating the fate and bioavailability of environmental (xeno)oestrogens (notably their transfer to benthic organisms and estuarine food chains), together with evidence for endocrine disruption in invertebrate populations.

Emphasis is placed on using published information to interpret the behaviour and effects of a small number of ‘model compounds’ thought to contribute to oestrogenic effects in nature; namely, the natural steroid 17β-oestradiol (E2) and the synthetic hormone 17α-ethinyloestradiol (EE2), together with the alkylphenols octyl- and nonyl-phenol (OP, NP) as oestrogen mimics. Individual sections of the review are devoted to sources and concentrations of (xeno)oestrogens in waterways, sediment partitioning and persistence, bioaccumulation rates and routes, assays and biomarkers of oestrogenicity, and, finally, a synopsis of reproductive and ecological effects in aquatic species.

Organotin (OT) compounds were determined in surface sediments and mussels Mytilus edulis from two major estuaries of the UK, the Mersey and the Thames, approximately one decade after legislation banning the use of tributyltin (TBT) compounds on small boats. Tributyltin concentrations in Mersey sediments ranged from 0·007–0·173 μg (as Sn) g−1 dry wt, increasing from the most upstream site, Fiddlers Ferry, towards the middle section of the estuary, and were highest at Stanlow, perhaps indicative of sources from the Manchester Ship Canal (MSC). A further peak in TBT concentrations occurred at New Brighton, opposite Liverpool Docks. Tributyltin was the predominant butyltin (BT) species in sediments (approximately 50%). Despite the fact that BTs represented only 4% of the total (HNO3-extractable) tin in sediments there was a linear relationship between these two tin compartments. Furthermore, BTs in mussels were correlative with total extractable tin in sediment, though in contrast to sediments, 85% of the total tin in mussels was made up of BTs, the most predominant of which was TBT. Concentrations of TBT in mussels increased from 0·058 μg Sn g−1 dry wt at the mouth of the estuary to 0·214 μg Sn g−1 dry wt at their upstream limit, close to the entrance to the MSC (Eastham). Triphenyltin (TPT) compounds were detected in only one sediment sample (New Brighton, 0·359 μg Sn g−1 dry wt) and one mussel population (Egremont, 0·022 μg Sn g−1 dry wt). Tributyltin concentrations in sediments from the Thames Estuary were marginally lower (0·002–0·078 μg Sn g−1 dry wt) than those found in the Mersey: highest concentrations were present in the upper estuary and decreased seaward. Again BTs contributed only a small percentage (<1% mean) towards the total tin loading in Thames sediments, but represented most of the tin burden (80%) in mussels. In contrast to sediments, TBT levels in mussels from the Thames Estuary were slightly higher than the Mersey (concentrations ranged from 0·100 μg Sn g−1 dry wt at the mouth to 0·302 μg Sn g−1 dry wt upstream) suggesting that TBT bioavailability is disproportionately higher in the Thames. Phenyltins were not detected in Thames samples.

Contaminants causing sex-altering, endocrine disrupting-like (ED) effects, or otherwise influencing reproduction, have been of growing concern to humans for more than 50 years. They have also been a perturbing, though less well-studied, phenomenon in marine organisms, following the recognition of tributyltin (TBT)-induced imposex and population extinctions in (neo)gastropods in the 1970s. Whilst ED impacts in mammals and fish are characterized by mimicry or antagonism of endogenous hormones by environmental contaminants (acting through Nuclear Receptors which are present in all metazoans) much less is known regarding pathways to effects in invertebrates. Despite the absence of a defined steroidal/mechanistic component, the extent, severity and widespread nature of ED-like manifestations and altered sexual characteristics observed in marine invertebrates gives rise to comparable concerns, and have been a long-term component of the MBA's research remit. The manifestations seen in sensitive taxa such as molluscs and crustaceans confirm they are valuable indicators of environmental quality, and should be exploited in this capacity whilst we seek to understand the pervasiveness and underlying mechanisms. In so doing, invertebrate indicators address aims of organizations, such as the EEA, OECD, UNEP and WHO, charged with management and monitoring of chemicals and ensuring that adverse effects on humans and the environment are minimized (Bergman et al., 2013). In view of the recent general declines in marine biodiversity, and the potential contribution of ED-like phenomena, safeguarding against deleterious effects through increased research which links pollutant exposure with reproductive dysfunction among invertebrates, is seen as a high priority.

The term ‘imposex’ was coined by Smith (1971) to describe the superimposition of male characters onto unparasitized and parasitized females of gonochoristic gastropods. In Nassarius obsoletus (Say) the development of imposex results in the female having one or more of the following characters: (1) a penis with a duct leading to (2) a vas deferens which passes back to the ventral channel of the capsule gland and (3) convolution of the normally straight gonadial oviduct (Smith, 1980). Imposex in the similarly gonochoristic Nucella lapillus (L.) was first noted by Blaber (1970) who found females with penis-like outgrowths in Plymouth Sound populations. Subsequent studies (Bryan et al. 1986; Gibbs & Bryan, 1986) have demonstrated that the incidence and intensity of imposex have since increased markedly in the same populations and that the phenomenon is widespread around south-west England.

Populations of the gastropod, Nucella lapillus (L.), normally one of the commonest of rocky-shore macroinvertebrates, have recently suffered from declining numbers at many sites along the south coast of England. Bryan et al. (1986) showed that these declining populations exhibited a high degree of imposex (the induction of a penis and vas deferens in females) and that imposex was almost certainly caused by tributyltin (TBT) compounds leached from ships' antifouling paints. Evidence implicating TBT compounds in the development of imposex included: (1) a good relationship between the degree of imposex and the proximity of affected populations to harbours and marinas; (2) in Plymouth Sound, the degree of imposex increased dramatically between its discovery in 1969 (Blaber, 1970) and 1985, thus coinciding with the introduction and increasing usage of TBT-based paints; (3) tissue concentrations of tin as TBT increased consistently with the degree of imposex; (4) animals transplanted from a ‘clean’ area to a harbour site absorbed TBT and developed imposex; (5) preliminary experiments showed that imposex was induced by exposure to 20 ng/1 of tin as TBT leached from a TBT-based paint; (6) TBT is implicated in the induction of imposex in other stenoglossan gastropods including Nassarius obsoletus (Say) (Smith, 1981) and Ocenebra erinacea (L.) (Féral & Gall, 1982).

A survey of the gastropod Nucella lapillus around the south-west peninsula of England has revealed that the incidence of ‘imposex’, the induction of male sex characters in the female, is widespread, that all populations are affected to some degree and that the phenomenon is most prevalent along the south (Channel) coast. Populations close to centres of boating and shipping activity show the highest degrees of imposex, especially those within the vicinities of the Helford, Fal, Salcombe and Dart estuaries and in Plymouth Sound and Tor Bay. Within Plymouth Sound the degree of imposex increased markedly between 1969 and 1985, coinciding with the introduction and increasing usage of antifouling paints containing tributyltin (TBT) compounds.

Rates of occurrence and degrees of imposex, and tissue concentrations of organotin compounds (tributyltin, TBT; dibutyltin, DBT; butyltin, MBT; triphenyltin, TPT; diphenyltin, DPT; and phenyltin, MPT) in the rock shell, Thais clavigera and T. bronni (Mollusca: Gastropoda) were investigated at 32 sites in Japan from May 1990 to October 1992. The rate of occurrence of imposex was 100% in both species, at almost all sites surveyed. Degrees of imposex indicated by relative penis length (RPL) index reflected the pollution levels not only of TBT, but also TPT. In heavily polluted areas, many individuals were found with oviducts which were blocked by vas deferens development, and capsule glands which were filled with aborted egg masses. These organisms were thought to be sterile.

Tributyltin (TBT) and its degradation products, dibutyltin (DBT) and monobutyltin (MBT), together with triphenyltin (TPT), were investigated in eels from the Thames Estuary and the Weston Canal (Merseyside). Within individual eels, the concentrations of organotin (OT) compounds varied considerably between tissues. Tributyltin concentrations were highest in heart and gall bladder and lowest in muscle and gonad. Tributyltin was generally the most predominant of butyltin (BT) compounds present in eel tissues and DBT the least. Phenyltins were detected in eels from both locations, notably the Weston Canal where TPT was present up to 0.367 μg g−1 (as Sn) in liver samples. Concentrations of OTs in liver (and muscle) were independent of weight and length in the eel populations examined. In a survey of OTs in eel populations along the Thames Estuary hepatic TBT levels ranged from 0.066–0.347 μg g−1 dry wt (as Sn) in liver of eels and were generally highest in the mid-section of the estuary, resembling the distribution pattern of TBT in sediment. Proportions of TBT to total BTs were also elevated in eel from this section of the waterway, consistent with continuing inputs in this region, albeit at relatively low levels. Major sewage treatment plants are sited here and may represent a possible source.

The susceptibility of marine bacterial communities to copper pyrithione (CuPT2), zinc pyrithione (ZnPT2) and their degradation product is described and toxicities of these relatively new antifouling biocides compared with those of their harmful organotin (OT) predecessors, tributyltin (TBT) and triphenyltin (TPT). These biocides were added to agar at concentrations of 0, 0.01, 0.1, 1 and 10 mg l−1 and coastal seawater including indigenous bacteria added to each batch of agar solution. The number of bacterial colony forming units (CFU) was measured after 7 days culture. Relative CFU (as a percentage of control) was more than 80% at a concentration of 0.01 mg l−1 of each compound, except for TBT. Relative CFU decreased as a function of dose of each biocide, although concentration-dependent changes in rate of CFU were relatively low during exposure to degradation products of CuPT2 and ZnPT2, pyridine N-oxide (PO) and pyridine-2-sulphonic acid (PSA). Based on comparisons of EC50, TBT was the most bacterio-toxic of the tested compounds (0.2 mg l−1), marginally more so than CuPT2 (0.3 mg l−1). Interestingly, EC50 values of degradation products of CuPT2 and ZnPT2, 2-mercaptopyridine N-oxide (HPT) and 2,2′-dithio-bispyridine N-oxide (PT2) were 0.8 and 0.5 mg l−1, respectively, lower than that of the parent chemical, ZnPT2 (1.4 mg l−1). The EC50 of PT2 was also lower than that of TPT (0.7 mg l−1), implying higher toxicity. Given the overlapping toxicity ranges, these results suggest that marine bacterial communities experience comparably high susceptibility to metal PTs and OTs during their life history.

The dogwhelk Nucella lapillus experienced localized extinction in the 1980s and 1990s due to the use of tributyltin (TBT) antifoulants, causing imposex in females. The aim of this study was to establish the extent of the return of the species across the mainland coast of central southern England as TBT use has been progressively restricted, and to quantify the extent of imposex impact on the populations present. We surveyed from Poole to Selsey where isolated populations had become extinct, and the Isle of Wight where some populations had persisted. We found evidence that since TBT restrictions, recolonization and colonization by N. lapillus has been rapid. By 2007–2008, of the eleven surveyed mainland sites, seven were colonized, although indications of reduced imposex impacts were mixed. Distribution had also extended on the Isle of Wight and populations were larger with less imposex impact in sites with long term populations. The lack of continuous suitable habitat blocks and the hydrodynamic complexity of the region, leads us to hypothesize that recovery has been facilitated by man-made structures which may be acting as ‘stepping stones’. Populations that have become established on engineered structures such as sea walls, breakwaters and rock groynes demonstrate accelerated recovery in the region as TBT in the environment has generally declined. Sites with suitable substrates and food sources near to ports were either not recolonized or had small populations with imposex evident. For species with a short pelagic larval stage or with direct development, population connectivity between patches of harder substrata along hydrodynamically complex coastlines may be greater than previously thought.

To examine the risk of transgenerational transfer of organotin compounds (OTs) in fish, tributyltin (TBT) and triphenyltin (TPT) compounds and their breakdown products were determined in both parental females and offspring of viviparous surfperch Ditrema temmincki collected from Japanese coastal waters. TBT concentrations (Mean ± SD) in the offspring (34 ± 5.7 ng Sn g−1 wet wt) were significantly higher (10–17 times) than in the parental females (2.8 ± 1.0 ng Sn g−1 wet wt). In the offspring, TBT was the predominant butyltin compound (82 ± 1.6% ∑BTs = TBT + DBT + MBT), and represented a greater proportion than in the parental females (51 ± 9.3% as TBT). TPT concentrations were significantly lower than TBT, and the ratio of TPT in parental females, relative to offspring, was different from TBT. TPT concentrations in the offspring (0.8 ± 0.3 ng Sn g−1 wet wt) were almost identical to those in the parental females (1.0 ± 0.5 ng Sn g−1 wet wt). TPT was the predominant phenyltin (∑PTs = TPT + DPT + MPT) in both offspring (73 ± 12% as TPT) and parental females (72 ± 18% as TPT). Results suggest that the transfer rate of TBT from parent to offspring could be much faster than its degradation rate in the offspring, accounting for higher accumulation of TBT in the latter. In contrast, the transfer rate of TPT is slower than its biodegradation, leading to a lower concentration of TPT in the offspring. It is therefore likely that the offspring might be at a higher risk from TBT than the parental females during their early growth stage in ovary in the viviparous surfperch whereas exposure to TPT is comparable in both generations.