Modulation of estrogenic effects by environmental temperature and food availability

Authors: FEIFAREK, DAVID - St Cloud State University; Shappell, Nancy; SCHOENFUSS, HEIKO - St Cloud State University

Submitted to: Meeting Abstract
Publication Type: Abstract Only
Publication Acceptance Date: 5/1/2014
Publication Date: 7/22/2014
Citation: Feifarek, D.J., Shappell, N.W., Schoenfuss, H.L. 2014. Modulation of estrogenic effects by environmental temperature and food availability [abstract]. 4th International Conference on Occurrence, Fate, Effects, and Analysis of Emerging Contaminants in the Environment, August 19-22, 2014, Iowa City, IA. Presented in Effects - III module: 9:45-10:00 a.m..

Interpretive Summary: Endocrine-disrupting chemicals (EDCs), in combination with environmental influences, interfere with endocrine function in humans and wildlife. Estrogens are a type of EDC that may alter the hypothalamic-pituitary-gonadal axis in male fathead minnows, Pimephales promelas. The impact of estrogens on P. promelas has been documented in previous laboratory exposures. Little is known, however, about the role the environment might play in modulating systemic upheaval resulting from estrogen exposure. A myriad of factors may influence estrogenic uptake and action. Due to this perplexity, the relevance of laboratory experiments is often questioned. To address the issue, we examined the effects of diet and temperature on male P. promelas exposed to the common estrogen, estrone (E1). Fish were exposed to either a low (14.25 ng/L) or high (71.45 ng/L) E1 concentration. Fish from both E1 treatments and a control group were exposed at either low (17.9°C) or high (26.3°C) water temperatures, and fed a restricted (0.75% body weight) or ad libitum (3% body weight) diet (12 groups, n = 20 fish per treatment) for 21 days. Analyses of biological endpoints including gonadosomatic index (GSI = gonad weight/whole body weight x 100), histopathology and plasma vitellogenin (VTG) concentration indicated statistical trends. The average GSI of fish exposed at a water temperature of 17.9°C was significantly greater than fish kept at 26.3°C, lending evidence to a potential evolutionary link between gonad weight and water temperature. This may allow for greater reproductive fitness in cold water throughout the range of P. promelas. Histopathological analysis of gonad tissues indicated that fish exposed at higher temperatures had significantly higher proportions of spermatozoa (mature male gametes). High prevalence of mature gametes, and the absence of early-stage gametes may indicate increased inhibitory influences on spermatogenesis at higher temperatures due to acceleration of metabolic factors involved in E1 uptake and action. Plasma VTG concentrations of control fish and those exposed to a low E1 treatment were not significantly different (166.19 µg/L and 310.99 µg/L, respectively). Fish exposed to a high E1 treatment had substantially higher plasma VTG concentrations (2108.35 µg/L). For this reason, plasma VTG analysis may not be a useful endpoint for environmental estrone concentrations below 14.25 ng/L. Furthermore, we anticipate that the incorporation of environmental factors into experimental designs may be a valid addition to laboratory studies in which aquatic toxicologists seek pertinent results with regards to their relevance in the natural environment of the model organism.

Technical Abstract: Endocrine-disrupting chemicals (EDCs), in combination with environmental influences, interfere with endocrine function in humans and wildlife. Estrogens are a type of EDC that may alter the hypothalamic-pituitary-gonadal axis in male fathead minnows, Pimephales promelas. The impact of estrogens on P. promelas has been documented in previous laboratory exposures. Little is known, however, about the role the environment might play in modulating systemic upheaval resulting from estrogen exposure. A myriad of factors may influence estrogenic uptake and action. Due to this perplexity, the relevance of laboratory experiments is often questioned. To address the issue, we examined the effects of diet and temperature on male P. promelas exposed to the common estrogen, estrone (E1). Fish were exposed to either a low (14.25 ng/L) or high (71.45 ng/L) E1 concentration. Fish from both E1 treatments and a control group were exposed at either low (17.9°C) or high (26.3°C) water temperatures, and fed a restricted (0.75% body weight) or ad libitum (3% body weight) diet (12 groups, n = 20 fish per treatment) for 21 days. Analyses of biological endpoints including gonadosomatic index (GSI = gonad weight/whole body weight x 100), histopathology and plasma vitellogenin (VTG) concentration indicated statistical trends. The average GSI of fish exposed at a water temperature of 17.9°C was significantly greater than fish kept at 26.3°C, lending evidence to a potential evolutionary link between gonad weight and water temperature. This may allow for greater reproductive fitness in cold water throughout the range of P. promelas. Histopathological analysis of gonad tissues indicated that fish exposed at higher temperatures had significantly higher proportions of spermatozoa (mature male gametes). High prevalence of mature gametes, and the absence of early-stage gametes may indicate increased inhibitory influences on spermatogenesis at higher temperatures due to acceleration of metabolic factors involved in E1 uptake and action. Plasma VTG concentrations of control fish and those exposed to a low E1 treatment were not significantly different (166.19 µg/L and 310.99 µg/L, respectively). Fish exposed to a high E1 treatment had substantially higher plasma VTG concentrations (2108.35 µg/L). For this reason, plasma VTG analysis may not be a useful endpoint for environmental estrone concentrations below 14.25 ng/L. Furthermore, we anticipate that the incorporation of environmental factors into experimental designs may be a valid addition to laboratory studies in which aquatic toxicologists seek pertinent results with regards to their relevance in the natural environment of the model organism.