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Feminisation of fish 8. Consequences of feminisation on the reproductive success/fertility of male fishAn important question which has been raised after the observations of reproductive disturbances in male fish in the environment is, whether these effects will have subsequent detrimental consequences for the fertility or reproductive capacity of the male fish and whether this will have effects on the population level. This question is difficult to answer based on the present observations. New results have recently been published on the reproductive health found among British intersex roach captured downstream of STPs (60). An asynchrony of gamete maturation among sexes was observed. When examined in autumn, in the middle of the reproductive cycle of the roach, the spermatogenesis was delayed in intersex and male fish from the sewage effluent receiving rivers and growth of the testes was inhibited in the most severely intersexed fish. In sewage effluent affected females, a higher incidence of oocyte atresia (degeneration) was found, and in both intersex males and females changed sex hormone levels were observed. When examined in spring around the time of spermiation only approximately 50 % of the males from the two sewage effluent receiving rivers were able to release sperm compared to 100 % spermiation among males from control sites. Further, those intersex fish which did spermiate had a reduced milt volume and a reduced sperm density. The lack of ability to spermiate could in some males be explained by observations of abnormalities in the sperm duct which could prevent the release of gametes. Female roach at this sampling time had already begun to spawn and these observations of asynchrony in the gamete maturation therefore indicate reduced reproductive success among the roach population from these rivers. In vitro fertilisation studies with gametes from roach taken from the effluent receiving rivers have supported this indication of reduced fertility (57). The viability of the gametes of wild roach was reduced for both male and female roach – but particularly for sperm and there was a negative correlation between the degree of intersex in an individual and the fertilisation success. In general the proportion of surviving embryos fell at each developmental stage but this pattern was magnified in embryos produced by severely intersexed fish. The factors that seemed to be responsible for the reduced male fertility among intersex fish were reduced sperm density, a lower proportion of motile sperm and reduced duration of sperm motility. The above mentioned studies are the only ones which yet have been performed to assess the effects of the observed feminisation on the reproductive capacity of wild male fish. A few studies with controlled exposure to estrogens and xenoestrogens have given some additional information as to whether these compounds have the potential to reduce the fertility. A fertilisation success below 70 % was observed in male zebrafish at exposure concentrations of 5-25 ng/l ethinylestradiol (61). In addition, the number of non-exposed females which spawned successfully when paired with exposed males was below the expected breeding success of non-exposed pairs. Therefore both the fertilisation success and the sexual behaviour of the exposed male zebrafish seemed to be impaired. At exposure to 10 and 25 ng/l EE2, significant reductions in the GSI, signalling altered spermatogenesis, were seen. This indicates that for some species such observations of inhibited testes development are indicatives of reduced fertility. A lower fertilisation rate (though not significant) has also been found for medaka when males exposed to OP (2-50 µg/l ) or E2 (100 ng/l) were paired with unexposed females (49). In male medaka exposed to a higher concentration of E2 (817 ng/l) for two weeks decreased or disappeared spermatogenesis was observed (62;63). Pairing the exposed males with unexposed females resulted in a decreased number of eggs laid by females and a decrease in the number of hatchlings. Bisphenol A caused a decrease in total egg number and hatchlings at a concentration of 2283 µg/l, while a decrease in the number of hatchlings was seen with 66 µg/l nonylphenol. In a similar study where male madaka was exposed to 20 – 280 µg/l octylphenol, unexposed females paired with these males produced approximately 50 % fewer eggs than the control group (191). Exposing both male and female rainbow trout to 10 m g NP/l for 10 days in each of 4 consecutive months prior to spawning resulted in reduced hatching rate of the F1 offspring due to high mortality of eggs before the eyed stage (51). A commonly observed feminisation in male fish which as described earlier has been observed in the field (and also in multiple controlled exposure experiments with estrogens and xenoestrogens) is the production of the female yolk protein, vitellogenin. The significance of this in relation to the reproductive capacity of the male fish is not known. Further, it is more difficult to interpret the importance of the vitellogenin production in males in relation to reproductive success than for instance a reduced capacity to fertilise eggs. High levels of vitellogenin in male fish have been reported to cause acute renal failure due to excessive accumulation of vitellogenin in the kidney since the male fish in contrast to females don’t have a target organ for the protein (64;65). Chronic exposure to lower concentrations of estrogenic chemicals might not cause the extensive liver and kidney pathologies as has been observed with high concentration exposures, but it has been proposed that a milder effect on the liver and kidney might result in a reduced ability to metabolise xenoestrogens or to resist diseases (65). Further, it has been suggested that vitellogenin production in males may decrease the part of metabolic consumption which is used for growth and spermatogenesis (66) and in females may result in altered calcium metabolism and therefore altered growth and bone formation in the embryos or larvae (201). A study by Gronen et al. 1999 has found a negative correlation between vitellogenin levels of octylphenol exposed male fish and percent fertilised eggs when these where paired with unexposed females (191). Both EE2 and NP have also been shown to cause severe anaemia in common carp exposed over a 70 day period to 500 µg/kg or 1 to 15 µg/l, respectively – supporting the fact, that a toxic response of a xenoestrogen or estrogen indirectly might influence the capacity left for sound reproduction due to an impairment of the general health condition of the fish.
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