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COLLAPSE OF A FISH POPULATION FOLLOWING EXPOSURE TO A SYNTHETIC ESTROGEN
Citation:
KIDD, K. A., P. J. BLANCHFIELD, K. H. MILLS, V. P. PALACE, R. E. EVANS, J. M. LAZORCHAK, AND R. W. FLICK. COLLAPSE OF A FISH POPULATION FOLLOWING EXPOSURE TO A SYNTHETIC ESTROGEN. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES. National Academy of Sciences, WASHINGTON, DC, 104(21):8897-8901, (2007).
Impact/Purpose:
The indeterminate condition of exposure indicator research stands to change markedly with the ability to connect molecular biological technologies with cellular or tissue effects and outcomes. Three focal areas of ecological research aim to develop a sequence of approaches where "the earliest recognizable signatures of exposure" (i.e., unique patterns of up- and down-regulated genes and proteins) are identified for numerous stressors, demonstrable in case studies and incorporated into Agency, State and Regional studies supported by EMAP and other programs. Area 1, Computational Toxicology Research: Exposure assessment has historically been based on use of chemical analysis data to generate exposure models. While biological activity of chemicals has been recognized to be important for exposure risk assessments, measurement of such activity has been limited to whole organism toxicity tests. Use of molecular approaches will: improve extrapolation between components of source-to-outcome continuum (source , exposure , dose , effect , outcome); Using a systems modeling approach, gene and protein expression data, in small fish models (fathead minnow and zebrafish), will be integrated with metabolomic and histopathological data. This will assist in prediction of environmental transformation and chemical effects based on structural characteristics, and enhance quantitative risk assessments, including areas of uncertainty such as a basis for extrapolation of effects of endocrine disrupting chemicals, interspecies extrapolation, complex chemical mixtures and dose-response assessment. Area 2, Ecological Research-Environmental Diagnostics: Development of molecular diagnostic indicators contributes to several of the GPRA Diagnostic Research Goals. Methods will employ DNA microarray technology and expression proteomics, focusing on species of relevance to aquatic ecosystem risk assessment. Significantly, these diagnostic indicators will open the door to understanding subcellular interactions resulting from exposure to complex chemical mixtures; define relationship between genetic disposition of populations and degree/specificity of stressor-specific gene transcriptional response in aquatic organisms (fish and invertebrates); identify chemical mixture induced transcriptional "patterns" using microarrays and hyperspectral scanning - via collaboration with DOE Sandia National Labs; apply molecular indicators to watershed level stressor study, including pilot studies with targeted pesticides and toxins indicators; develop molecular indicators of exposure for invertebrates (Daphnia, Lumbriculus, Chironomus); Area 3, Exposure Research in Endocrine Disruptors: Subobjective 1: Develop exposure methods, measurement protocols, and models for assessment of risk management practices of endocrine disrupting compounds. As risk management approaches are identified and developed, there will be a need to identify, adapt and develop bioassay screening tools and other analytical methods to assess their efficacy. Measurements research will be performed to define management needs. This effort will entail cross-lab participation from NRMRL, NERL and NHEERL. Subobjective 2: Determine extent of environmental and human exposures to EDCs, characterize sources and factors influencing these exposures, develop and evaluate risk management strategies to reduce exposures. In order to develop effective risk management strategies, it is important to understand the extent of exposures to endocrine disrupting compounds and factors influencing source-to-exposure-to-dose relationships; apply molecular indicators of exposure to estrogenic compounds in selected wastewater treatment plants located in ten USEPA Regions; identify differential gene expression following exposure of fathead minnows to environmental androgens and androgen-like compounds; apply molecular indicators of exposure to estrogenic and androgenic compounds present in CAFO studies - linkage to chemistry and
Description:
Municipal wastewaters are a complex mixture containing estrogens and estrogen mimics that are known to affect the reproductive health of wild fishes. Male fishes downstream of some wastewater outfalls produce vitellogenin (VTG) (a protein normally synthesized by females during oocyte maturation) and early stage eggs in their testes, and this feminization has been attritubed to the presence of estrogenic substances such as natural estrogens, the synthetic estrogen used in birth control pills, or weaker estrogen mimics such as nonylphenol in water. Despite widespread evidence that male fishes are being feminized, it is not known whether these low-level, chronic exposures adversely impact the sustainability of wild populations. We conducted a seven year whole-lake experiment at the Experimental Lakes Area (ELA) in northwestern Ontario, Canada and showed that chronic exposure of fathead minnow (Pimephales promelas) to low concentrations of the potent EE2 led to feminization of males through the production of VTG mRNA and protein, impacts on gonadal development as evidenced by intersex in males and altered oogenesis in females, and, ultimately, a near extinction of this species from the lake. Our observations demonstrate that the concentrations of estrogens and their mimics observed in freshwaters can impact the sustainability of wild fish populations.