Linkage of biochemical responses to population‐level effects: A case study with vitellogenin in the fathead minnow (Pimephales promelas)

A challenge in the field of ecotoxicology is the linkage of alterations at molecular and biochemical levels of organization to adverse outcomes in individuals and populations. In the present study, a predictive relationship between plasma vitellogenin (VTG) concentration and fecundity in female fathead minnows (Pimephales promelas) was derived from 21-d laboratory toxicity tests with five chemicals (17beta-trenbolone, 17alpha-trenbolone, prochloraz, fenarimol, and fadrozole) that inhibit VTG production through different mechanisms. Because VTG is key to egg production in female oviparous animals, changes in the lipoprotein could, theoretically, serve as an indicator of reproductive success. Regression of fecundity versus VTG concentration from the various studies yielded a highly significant linear model (fecundity = -0.042 + 0.95 x VTG, p < 0.01, r2 = 0.88). This relationship was integrated into a population model to translate changes in VTG concentrations of female fathead minnows to alterations in population growth. The model predicted relatively profound effects on population size of fish experiencing moderate decreases in vitellogenesis. For example, a fathead minnow population at a carrying capacity exposed to a chemical stressor that causes a 25% decrease in VTG concentration in females from baseline values would exhibit a 34.6% projected decrease in size after two years of exposure and reach an equilibrium population size that was only 30.2% of the preexposed population. Overall, the current study provides an example of how changes in a biomarker (VTG concentration) can be quantitatively translated into adverse effects at the individual and population levels.

[1]  J. W. Arthur,et al.  Acidification effects on macroinvertebrates and fathead minnows (Pimephales promelas) in outdoor experimental channels , 1983 .

[2]  R. Huggett,et al.  Biomarkers: Biochemical, Physiological, and Histological Markers of Anthropogenic Stress , 1992 .

[3]  Gerald T Ankley,et al.  Evaluation of the aromatase inhibitor fadrozole in a short-term reproduction assay with the fathead minnow (Pimephales promelas). , 2002, Toxicological sciences : an official journal of the Society of Toxicology.

[4]  J. Sumpter,et al.  Oocyte growth and development in teleosts , 1996, Reviews in Fish Biology and Fisheries.

[5]  Cheryl A Murphy,et al.  Modeling vitellogenesis in female fish exposed to environmental stressors: predicting the effects of endocrine disturbance due to exposure to a PCB mixture and cadmium. , 2005, Reproductive toxicology.

[6]  Gerald T Ankley,et al.  Effects of the androgenic growth promoter 17‐β‐trenbolone on fecundity and reproductive endocrinology of the fathead minnow , 2003, Environmental toxicology and chemistry.

[7]  R. Haight,et al.  A Regional Landscape Analysis and Prediction of Favorable Gray Wolf Habitat in the Northern Great Lakes Region , 1995 .

[8]  L. Folmar,et al.  Vitellogenin-induced pathology in male summer flounder (Paralichthys dentatus). , 2001, Aquatic toxicology.

[9]  P. Holgate,et al.  Matrix Population Models. , 1990 .

[10]  D. Nacci,et al.  Risks of Endocrine-Disrupting Compounds to Wildlife: Extrapolating from Effects on Individuals to Population Response , 2001 .

[11]  M. Mcmaster,et al.  An Epidemiological Evaluation of the Biochemical Basis for Steroid Hormonal Depressions in Fish Exposed to Industrial Wastes , 1996 .

[12]  Kunio Kobayashi,et al.  Comparison of response to 17β‐estradiol and 17β‐trenbolone among three small fish species , 2006 .

[13]  R. Haight,et al.  Causes and Implications of Species Restoration in Altered Ecosystems , 1997 .

[14]  G. Ankley,et al.  Fathead minnow vitellogenin: Complementary DNA sequence and messenger RNA and protein expression after 17β‐estradiol treatment , 2000 .

[15]  Valery E Forbes,et al.  The use and misuse of biomarkers in ecotoxicology , 2006, Environmental toxicology and chemistry.

[16]  Nicholas J. Gotelli,et al.  A Primer of Ecology , 1995 .

[17]  M. Ricci,et al.  Further Insights Into The Potential Of Pulp And Paper Mill Effluents To Affect Fish Reproduction , 2005, Journal of toxicology and environmental health. Part A.

[18]  Mark Crane,et al.  Vitellogenin: A Review of Analytical Methods to Detect (Anti) Estrogenic Activity in Fish , 2005, Toxicology mechanisms and methods.

[19]  Demetrio Raldúa,et al.  First evidence of endocrine disruption in feral carp from the Ebro River. , 2004, Toxicology and applied pharmacology.

[20]  J. Parrott.  Overview of methodology and endpoints in fathead minnow lifecycle tests assessing pulp and paper mill effluents , 2005 .

[21]  L. Gray,et al.  Evaluation of the model anti-androgen flutamide for assessing the mechanistic basis of responses to an androgen in the fathead minnow (Pimephales promelas). , 2004, Environmental science & technology.

[22]  Grace H Panter,et al.  Utility of a juvenile fathead minnow screening assay for detecting (anti‐)estrogenic substances , 2002, Environmental toxicology and chemistry.

[23]  Maria Linderoth,et al.  Altered steroid metabolism in several teleost species exposed to endocrine disrupting substances in refuse dump leachate. , 2003, General and comparative endocrinology.

[24]  J. Sumpter,et al.  Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. , 1995, Environmental health perspectives.

[25]  Gerald T Ankley,et al.  Modeling impacts on populations: fathead minnow (Pimephales promelas) exposure to the endocrine disruptor 17beta-trenbolone as a case study. , 2004, Ecotoxicology and environmental safety.

[26]  G. Ankley,et al.  Screening and Testing for Endocrine Disruption in Fish—Biomarkers As “Signposts,” Not “Traffic Lights,” in Risk Assessment , 2005, Environmental health perspectives.

[27]  Terri Damstra,et al.  Global assessment of the state-of-the-science of endocrine disruptors , 2002 .

[28]  J. D. Winter,et al.  Biology and Ecology of Fishes , 1995 .

[29]  P. H. Leslie.  On the use of matrices in certain population mathematics. , 1945, Biometrika.

[30]  Daniel L Villeneuve,et al.  The fathead minnow in aquatic toxicology: past, present and future. , 2006, Aquatic toxicology.

[31]  Gerald T Ankley,et al.  Effects of the feedlot contaminant 17alpha-trenbolone on reproductive endocrinology of the fathead minnow. , 2006, Environmental science & technology.

[32]  G. Ankley,et al.  Description and evaluation of a short‐term reproduction test with the fathead minnow (Pimephales promelas) , 2001, Environmental toxicology and chemistry.

[33]  L. Gray,et al.  Effects of two fungicides with multiple modes of action on reproductive endocrine function in the fathead minnow (Pimephales promelas). , 2005, Toxicological sciences : an official journal of the Society of Toxicology.

[34]  Anders Goksøyr,et al.  Eggshell and egg yolk proteins in fish: hepatic proteins for the next generation: oogenetic, population, and evolutionary implications of endocrine disruption , 2003, Comparative hepatology.