Hormones and endocrine disrupters in aquatic environment

Abstract

The UK's programme on endocrine disruption in the marine environment (EDMAR) was set up in 1998 to investigate in more detail the implications of earlier observations of strongly oestrogenic effects in flounder (Platichthys flesus) from several UK estuaries. Much of the work has focused on fish, including further studies of flounder, as well as investigations of sand gobies (Pomatoschistus minutus and P. lozanoi) and viviparous blennies (Zoarces viviparous). Some work has also begun to investigate androgenic effects in the stickleback (Gasterosteus aculeatus). There have in addition been detailed chemical studies to identify the sources and types of oestrogenic substances. The additional work with flounder has confirmed the original findings that many industrialised UK estuaries are sufficiently oestrogenic to cause strong induction of yolk protein (vitellogenin or VTG) in male fish (by up to a million‐fold in excess of controls), as well as induction of intersex (ovotestis) in some male individuals (15–20% in some areas). Although the levels of activity at some sites have not changed significantly over 3 years, VTG titres have decreased at other sites, perhaps due to improvements in sewage treatment, although these findings need confirmation over a longer timespan. Experiments with male flounder showed that they did not produce VTG when caged in oestrogen‐contaminated estuaries, but experienced mild VTG induction when fed on mussels (Mytilus edulis) which had been held in an oestrogen‐contaminated estuary (the Tees) for 3 months. This shows that at least some oestrogenic substances have the potential for transmission through the food chain. Studies of the viviparous blenny have shown that, like in flounder, males are producing VTG (measured as VTG mRNA) in some estuaries, and up to 25% of male fish are showing intersex (ovotestis). Studies are under way to investigate whether this is affecting the production of fry in this species. Viviparous blennies are ideal for such work because the fry produced by each individual wild female can be directly counted and measured. Sand gobies from oestrogen‐contaminated estuaries did not show either induction of VTG mRNA or intersex, even though the former could be induced in the laboratory through exposure to reference oestrogens. However, high proportions of male gobies from oestrogen‐contaminated locations such as the Mersey and Tees showed a condition of the urogenital papilla (UP) in which the terminal part of this organ had grown villae resembling those seen on female papillae. The UP is used by both sexes to deposit gametes, and it is possible that the apparent feminisation seen in oestrogen‐ exposed males could interfere with normal reproduction. Experiments are in progress to attempt to replicate the condition (known as Male Intermediate Papilla Syndrome ‐ MIPS) in oestrogen‐exposed fish. The EDMAR programme has developed a biomarker of androgenic exposure, the glue protein spiggi, which is induced in female sticklebacks when they are exposed to exogenous androgens. Preliminary work has shown that there is only limited androgenic activity induced in female fish held in the Tees. However, a range of natural androgens has been detected in certain sewage discharges. Work is also progressing to investigate the possible effects of estuarine endocrine disrupters on smoltification in salmon. Finally, the yeast oestrogen screen (YES) has been used in a Toxicity Identification and Evaluation (TIE) scheme to identify substances probably causing these effects. The majority of oestrogenic activity in sewage effluents and estuarine waters has been attributable to oestradiol, although a small proportion is being caused by other natural steroids, as well as synthetic substances such as nonylphenol. However, the overwhelming majority of the activity in the investigated estuaries (Tees and Tyne) is to be found in the sediments. Most of the sediment‐bound activity remains to be identified, but little appears to be attributable to oestradiol. Although the EDMAR programme will only reach completion at the end of 2001, it is already apparent that oestrogenic effects are very widespread in 4 fish species from several industrialised UK estuaries. It appears that the sediments can become heavily contaminated with certain oestrogens, and it seems likely that fish become contaminated at least partly via consumption of benthic invertebrates. However, the full ecological implications of the effects observed in fish have not yet been fully elucidated.