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Title: Oestrogenic endocrine disruption in flounder (Platichthys flesus L.) from United Kingdom estuarine and marine waters
Author: P. Matthiessen
Author: Y. T. Allen
Author: C. R. Allchin
Author: S. W. Feist
Author: M. F. Kirby
Author: R. J. Law
Author: A. P. Scott
Author: J. E. Thain
Author: K. V. Thomas
Author: Burnham on Crouch CEFAS:
Document Type: Monograph
Annotation: Environment Agency Project ID:EAPRJOUT_349, Representation ID: 86, Object ID: 1694
be significantly elevated (in comparison with a clean reference site on the Alde estuary) in at least one sample from most of the 11 estuaries investigated. The exceptions were the Tamar and the Dee where fish appeared entirely normal. In broad terms, the degree of oestrogenic contamination as measured by male vitellogenesis in the various estuaries can be ranked in the following descending order: Tees > Mersey >ATyne > Wear = Humber = Clyde = Southampton Water = Thames > Crouch > Dee =ATamar. VTG concentrations in Tees, Mersey and Tyne fish were extremely high (>100,000 ng ml-1), and often exceeded those normally found in sexually mature females. There were no major differences between VTG levels measured in 1996/97 and 1997/98. 1.1 This report describes one aspect of a phenomenon known as endocrine disruption (ED) which concerns the interference of environmental chemicals with the normal functioning of the endocrine (hormone) system. The aspect considered is that of substances in the UK marine environment which are able to mimic female vertebrate hormones (oestrogens) such as 17Ioestradiol, and thereby cause inappropriate feminisation of male fish (and other organisms). 1.2 It is already known that natural and synthetic oestrogenic hormones, and at least one industrial chemical, in sewage treatment works (STW) discharges are causing widespread feminisation of male river fish in the UK. This feminisation involves the unnatural synthesis of the yolkprecursor protein vitellogenin (VTG), and the induction of a condition known as ovotestis, in which egg cells develop in otherwise normal testes. Fish with this condition are described as AintersexA although they remain genetically male. It is thought that this process may be damaging the ability of some freshwater fish to breed, but this has not yet been unequivocally established. 1.6 Flounder were also sampled from 5 coastal sites, and from several sites in the central southern North Sea. In all cases, VTG was significantly induced, and in the case of fish from Liverpool Bay and Red Wharf Bay (Anglesey), the degree of induction was large (although not as large as in the Mersey). Laboratory experiments indicated that VTG in male fish disappears rather slowly, with a half-life of about 2 weeks, and it is therefore suggested that the high VTG in fish at these two sites could have been induced in an estuary (probably the Mersey) before they migrated to sea to breed. However, local oestrogenic contamination at coastal and offshore sites cannot be entirely ruled out. 1.3 The present investigation set out to look for similar effects in the sea, and has focused on a common estuarine flatfish, the flounder (Platichthys flesus L.). This species, although not the basis of a significant fishery in the UK, was considered suitable for this survey because it is heavily exposed to contaminants associated with the muddy sediments in which it lives. Furthermore, it spends most of its life in its home river and estuary, only venturing offshore to breed. This means that studying feminisation in flounder will reveal something about the geographical location of the oestrogenic discharges which are contributing to any effects. 1.7 At most locations, ovotestis conditions in male flounder were entirely absent. However, in 1996, 17% of Mersey fish showed this abnormality, with large numbers of primary and secondary egg cells (oocytes) in the testes. In 1997, 9% of male Mersey fish and 7% of male Tyne fish contained ovotestis. In a few cases, eggs were fully developed with yolk granules. Most testes did not show gross morphological abnormalities related to oestrogenic exposure, although one testis from the Mersey appeared to be almost entirely composed of eggs. Unexpectedly, in view of the high levels of VTG induction, no intersex fish were seen in the Tees, but this is probably due to the fact that the sample size from this estuary was very small. Broadly speaking, ovotestis only seems to occur in flounder populations when mean plasma VTG levels in male adults exceed 100,000 ng ml-1. 1.4 The primary techniques used in this survey included the measurement of VTG in male and female flounder, a search for feminised testes and other intersex conditions, and measurement of gonadal weights and sex ratios. Supplementary information was provided by chemical analysis for a range of contaminants in flounder liver tissue, measurement of certain steroid hormones in flounder, and measurement of the degree of induction of the cytochrome P450 mixedfunction oxidase enzymes, a major system by means of which fish are able to degrade and excrete unwanted substances. 1.8 Abnormal sex ratios were not seen in any estuary, although this is based on histological and not genetic data; i.e. it is possible that some of the overt females may have been genetic males. There was no consistent pattern to the distribution of testis:body weight ratios (i.e. gonadosomatic 1.5 Vitellogenin levels in male blood plasma in the period autumn 1996 to spring 1998 were found to 5 ratio), but hepatosomatic ratios (i.e. liver:body weight) were increased in males which had elevated VTG. This shows that oestrogenic exposure had caused abnormal liver growth (hypertrophy) in order to synthesise VTG, thus placing strain on the metabolism of these fish. materials are almost certainly contributing to the observed effects. There is little correlation between VTG induction and the volumes of domestic sewage discharged to each estuary, but there is a much clearer relationship with the volume of industrial effluent. Again, this does not prove a causal link with industrial chemicals, but it suggests that non-hormonal substances are major players. 1.9 Due to resource limitations, only female Dee estuary flounder were sampled for natural steroid hormones (in September 1997). Male hormones (the androgens 11-ketotestosterone and testosterone) were not detectable, while the oestrogen 17I-oestradiol was only present at a low level in one fish. This was probably due to the season of sampling, and it would be desirable to conduct more analyses of this type in order to establish whether hormone metabolism is altered in the more oestrogen-contaminated fish. 1.13 The full biological implications of these results are not yet understood, but it is a possibility that flounder in the most contaminated estuaries (Tees, Mersey, Tyne) have impaired reproductive output and reduced overall fitness. Whether this is likely to have long-term implications for the survival of these flounder populations is unknown, but it seems unlikely that flounder in the UK as a whole are seriously endangered from oestrogenic exposure. However, it should be noted that the most oestrogen-sensitive part of the flounderAs life cycle (the larva undergoing gonad formation) occurs at sea where contaminant levels are relatively low. It is therefore likely that species which breed in estuaries will be experiencing more serious effects. 1.10 The pattern of induction of the P450 mixed function oxidase system in flounder liver (as measured by the activity of the enzyme ethoxyresorufin-o-deethylase, or EROD) showed considerable similarities with the pattern of VTG induction, with highest EROD activity in the Mersey, Tees and Tyne, intermediate activity in the Humber, Wear and Southampton Water, and low activity in the Alde reference site. It is possible that the EROD was being induced by the same substances responsible for oestrogenicity, but even if not, there may still be reproductive implications because the P450 system is responsible for metabolising steroids. The main EROD inducers are the planar polychlorinated biphenyls (PCBs), polychlorinated dibenzodioxins and furans (PCDDs and PCDFs), and polycyclic aromatic hydrocarbons (PAHs), several of which are known to have endocrine disrupting properties. 1.14 It is recommended that further research is conducted in order to clarify the following:a What are the major oestrogenic substances in UK estuaries and what are the main sources? a What are the implications for the reproductive output (and hence for populations) of fish species which breed in the more contaminated situations? a What impacts are oestrogens having on the reproductive output of other estuarine organisms (e.g. crustaceans and molluscs)? a Are UK estuaries significantly contaminated with other endocrine disrupters such as androgen and thyroid hormone mimics, and their antagonists? 1.11 In broad terms, the flounder from the Mersey and Tees were the most contaminated with organochlorines and PAHs, although appreciable amounts of PCBs were also present in Thames and Tamar fish. However, the levels of these contaminants in liver were rather low (max. median IPCB = 1.3 mg kg-1 wet wt.; max. median IDDT = 0.5 mg kg-1 wet wt.; max. IPAH = 0.4 mg kg-1 wet wt.). It is doubtful whether these residues made a major positive or negative contribution to the observed oestrogenic effects, but they at least indicate that the fish which were most contaminated with common manmade chemicals were also those most impacted by oestrogenic hormones and/or their mimics. It is clear that more investigative chemistry is required to identify the causative compounds. Many of these questions are being addressed by a new 4-year research programme (Endocrine Disruption in the Marine Environment, or EDMAR) funded mainly by the British Government (Ministry of Agriculture, Fisheries and Food A MAFF; Department of Environment, Transport and the Regions A DETR; Environment Agency A EA; Scotland and Northern Ireland Forum for Environmental Research A SNIFFER), but also by the European Chemical Industry Association (CEFIC). The programme is being managed by the Centre for Environment, Fisheries and Aquaculture Science (CEFAS), but other collaborating organisations include Fisheries Research Services (FRS) Marine Laboratory, Aberdeen, Zeneca Brixham Environmental Laboratory, and the Universities of Liverpool and Plymouth. 1.12 It seems unlikely that the major causative substances will prove to be oestrogenic hormones derived from domestic sewage, although these 6 2.
Publisher: Environment Agency
Subject Keywords: Marine pollution; Oestrogens; Endocrine distrupter; Fishes
Extent: 52
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