In a previous post, I wrote about vitellogenin genes, which are expressed in the liver to produce yolk proteins for developing eggs, maturing within the ovaries of non-mammalian vertebrates. Transcription of vitellogenin genes is responsive to estrogen, allowing coordination of egg production with the breeding cycle of the animal. Unfortunately, the prevalence of estrogens and estrogen-like compounds in municipal wastewater or effluents can disturb this cycle, and adversely affect the production of sperm in male fish, as well as the production of eggs in female fish. The presence of intersex fish, with feminized reproductive ducts and eggs developing in their testes, is correlated with proximity to sewage discharge sites. Studies in a variety of estuarine and freshwater fish species have documented the ability of natural and synthetic estrogens to cause abnormal vitellogenin gene expression, which disrupts the reproductive physiology of both male and female fish (Jobling et al., 2006).
Fathead Minnow, Pimephales promelas
Image source: Wikipedia
To examine the effects of estrogens and estrogen mimics on a common freshwater fish, the Fathead Minnow, Kidd and colleagues (2007) set up a seven-year study of populations of these fish in experimental lakes. In the test lake, the researchers used a potent synthetic estrogen, 17α-ethynylestradiol (EE2), to replicate estrogen concentrations present in municipal wastewaters; the reference lake received no added estrogens. Vitellogenin mRNA and protein levels were measured in both male and female fish at several different time points, and as expected, EE2 both increased and prolonged expression of vitellogenin in the test lake minnows. Male fished exposed to EE2 showed intersex characteristics, with developing eggs in the testes, as well as immature and abnormal sperm cells. Female minnows from the test lake were also affected by the increased estrogen levels, and their ovaries contained atretic (dying) follicles, and the maturation of egg cells was delayed.
The key finding in this paper, however, arises from the yearly population monitoring in the test and reference lakes, because these analyses revealed the long-term consequences of estrogen exposure. Over the 7-year study period, Kidd and colleagues used index trap netting to measure the minnow population size and structure, or age composition (determined by fish body length). They found that in the third season of estrogen level manipulations, the Fathead Minnow population collapsed in the test lake, reflecting a loss of smaller individuals, the young-of-the-year. The reproductive failure and population collapse are dramatic in a short-lived species, such as the Fathead Minnow, and the population collapse has not yet been observed by the researchers for the longer-lived Pearl Dace, Margariscus margarita. Nevertheless, the serious effects of wastewater estrogens on fish reproductive physiology could cause population declines for many different species.
Jobling, S., Williams, R., Johnson, A., Taylor, A., Gross-Sorokin, M., Nolan, M., Tyler, C.R., van Aerle, R., Santos, E., and Brighty, G. (2006). Predicted exposures to steroid estrogens in UK rivers correlate with widespread sexual disruption in wild fish populations. Environmental Health Perspectives 114 (Suppl. 1), 32-39.
Kidd, K.A., Blanchfield, P.J., Mills, K.H., Palace, V.P., Evans, R.E., Lazorchak, J.M., Flick, R.W. (2007). Collapse of a fish population after exposure to a synthetic estrogen. Proceedings of the National Academy of Sciences, 104(21), 8897-8901. DOI: 10.1073/pnas.0609568104