From 'omics to otoliths: responses of an estuarine fish to endocrine disrupting compounds across biological scales.

Endocrine disrupting chemicals (EDCs) cause physiological abnormalities and population decline in fishes. However, few studies have linked environmental EDC exposures with responses at multiple tiers of the biological hierarchy, including population-level effects. To this end, we undertook a four-ti...

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Main Authors: Susanne M Brander, Richard E Connon, Guochun He, James A Hobbs, Kelly L Smalling, Swee J Teh, J Wilson White, Inge Werner, Michael S Denison, Gary N Cherr
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3783432?pdf=render
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spelling doaj-96df991b067d44e19bfbd761a82305602020-11-25T00:48:22ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0189e7425110.1371/journal.pone.0074251From 'omics to otoliths: responses of an estuarine fish to endocrine disrupting compounds across biological scales.Susanne M BranderRichard E ConnonGuochun HeJames A HobbsKelly L SmallingSwee J TehJ Wilson WhiteInge WernerMichael S DenisonGary N CherrEndocrine disrupting chemicals (EDCs) cause physiological abnormalities and population decline in fishes. However, few studies have linked environmental EDC exposures with responses at multiple tiers of the biological hierarchy, including population-level effects. To this end, we undertook a four-tiered investigation in the impacted San Francisco Bay estuary with the Mississippi silverside (Menidia audens), a small pelagic fish. This approach demonstrated links between different EDC sources and fish responses at different levels of biological organization. First we determined that water from a study site primarily impacted by ranch run-off had only estrogenic activity in vitro, while water sampled from a site receiving a combination of urban, limited ranch run-off, and treated wastewater effluent had both estrogenic and androgenic activity. Secondly, at the molecular level we found that fish had higher mRNA levels for estrogen-responsive genes at the site where only estrogenic activity was detected but relatively lower expression levels where both estrogenic and androgenic EDCs were detected. Thirdly, at the organism level, males at the site exposed to both estrogens and androgens had significantly lower mean gonadal somatic indices, significantly higher incidence of severe testicular necrosis and altered somatic growth relative to the site where only estrogens were detected. Finally, at the population level, the sex ratio was significantly skewed towards males at the site with measured androgenic and estrogenic activity. Our results suggest that mixtures of androgenic and estrogenic EDCs have antagonistic and potentially additive effects depending on the biological scale being assessed, and that mixtures containing androgens and estrogens may produce unexpected effects. In summary, evaluating EDC response at multiple tiers is necessary to determine the source of disruption (lowest scale, i.e. cell line) and what the ecological impact will be (largest scale, i.e. sex ratio).http://europepmc.org/articles/PMC3783432?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Susanne M Brander
Richard E Connon
Guochun He
James A Hobbs
Kelly L Smalling
Swee J Teh
J Wilson White
Inge Werner
Michael S Denison
Gary N Cherr
spellingShingle Susanne M Brander
Richard E Connon
Guochun He
James A Hobbs
Kelly L Smalling
Swee J Teh
J Wilson White
Inge Werner
Michael S Denison
Gary N Cherr
From 'omics to otoliths: responses of an estuarine fish to endocrine disrupting compounds across biological scales.
PLoS ONE
author_facet Susanne M Brander
Richard E Connon
Guochun He
James A Hobbs
Kelly L Smalling
Swee J Teh
J Wilson White
Inge Werner
Michael S Denison
Gary N Cherr
author_sort Susanne M Brander
title From 'omics to otoliths: responses of an estuarine fish to endocrine disrupting compounds across biological scales.
title_short From 'omics to otoliths: responses of an estuarine fish to endocrine disrupting compounds across biological scales.
title_full From 'omics to otoliths: responses of an estuarine fish to endocrine disrupting compounds across biological scales.
title_fullStr From 'omics to otoliths: responses of an estuarine fish to endocrine disrupting compounds across biological scales.
title_full_unstemmed From 'omics to otoliths: responses of an estuarine fish to endocrine disrupting compounds across biological scales.
title_sort from 'omics to otoliths: responses of an estuarine fish to endocrine disrupting compounds across biological scales.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2013-01-01
description Endocrine disrupting chemicals (EDCs) cause physiological abnormalities and population decline in fishes. However, few studies have linked environmental EDC exposures with responses at multiple tiers of the biological hierarchy, including population-level effects. To this end, we undertook a four-tiered investigation in the impacted San Francisco Bay estuary with the Mississippi silverside (Menidia audens), a small pelagic fish. This approach demonstrated links between different EDC sources and fish responses at different levels of biological organization. First we determined that water from a study site primarily impacted by ranch run-off had only estrogenic activity in vitro, while water sampled from a site receiving a combination of urban, limited ranch run-off, and treated wastewater effluent had both estrogenic and androgenic activity. Secondly, at the molecular level we found that fish had higher mRNA levels for estrogen-responsive genes at the site where only estrogenic activity was detected but relatively lower expression levels where both estrogenic and androgenic EDCs were detected. Thirdly, at the organism level, males at the site exposed to both estrogens and androgens had significantly lower mean gonadal somatic indices, significantly higher incidence of severe testicular necrosis and altered somatic growth relative to the site where only estrogens were detected. Finally, at the population level, the sex ratio was significantly skewed towards males at the site with measured androgenic and estrogenic activity. Our results suggest that mixtures of androgenic and estrogenic EDCs have antagonistic and potentially additive effects depending on the biological scale being assessed, and that mixtures containing androgens and estrogens may produce unexpected effects. In summary, evaluating EDC response at multiple tiers is necessary to determine the source of disruption (lowest scale, i.e. cell line) and what the ecological impact will be (largest scale, i.e. sex ratio).
url http://europepmc.org/articles/PMC3783432?pdf=render
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