From ‘Omics to Otoliths: Responses of an Estuarine Fish to Endocrine Disrupting Compounds across Biological Scales

Abstract

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).

Contaminant Effects on California Bay–Delta Species and Human Health

“…Multiple-species studies that evaluated BayDelta ambient water samples, or conducted in situ exposures (referenced in Table 1), have repeatedly identified a broad set of mechanistic, systemic (immune, neurological, endocrine), histopathological (tissue damage), and whole-organism effects (e.g., growth, development, deformities). Endocrinedisruptive effects have been measured in samples from Sacramento River tributaries and in the BayDelta (Schlenk et al 2012;Brander et al 2013;.…”

“…Although identification of chemical classes responsible for these effects is limited, because of the complexities resulting from mixtures of multiple chemicals, several studies (see Table 1) have highlighted pyrethroid pesticides as responsible for toxicity, endocrine disruption, and neurological impairments in both fish and their prey (Brander et al 2013(Brander et al , 2016bHasenbein et al 2015c;Jeffries et al 2015b;Weston et al 2015a). …”

“…Population growth rates of Delta species are affected by exposure to contaminants (Brooks et al 2012). Recent research 12 VOLUME 14, ISSUE 4, ARTICLE 5 conducted in the Delta determined that contaminants sourced via water treatment plants disrupt endocrine system function in Inland Silversides (Menidia beryllina), resulting in alterations to gonado-somatic indices (GSI), testicular necrosis, and biased sex ratios (Brander et al 2013). Adult Inland Silversides exposed to low, Delta-relevant concentrations (0.5 ng L -1 ) of the pyrethroid bifenthrin had a significant reduction in reproductive output and biased sex ratios (fertilized eggs per female; Brander et al 2013Brander et al , 2016b.…”

“…Recent research 12 VOLUME 14, ISSUE 4, ARTICLE 5 conducted in the Delta determined that contaminants sourced via water treatment plants disrupt endocrine system function in Inland Silversides (Menidia beryllina), resulting in alterations to gonado-somatic indices (GSI), testicular necrosis, and biased sex ratios (Brander et al 2013). Adult Inland Silversides exposed to low, Delta-relevant concentrations (0.5 ng L -1 ) of the pyrethroid bifenthrin had a significant reduction in reproductive output and biased sex ratios (fertilized eggs per female; Brander et al 2013Brander et al , 2016b. Risks associated with exposure to endocrine-disrupting compounds (EDCs), have been extensively reviewed (Bortone and Davis 1994;Tyler et al 1998;Brander et al 2013Brander et al , 2016a.…”

Perspectives on Bay–Delta Science and Policy

“…Bio-markers are particularly useful as part of a weight-of-evidence approach, and are informative for understanding mechanisms behind sublethal organismal responses, such as behavioral alterations. Bio-markers have been used by generations of epidemiologists, physicians, and scientists to study human disease and have been employed in the Delta to detect physiological response to endocrine disruptors (e.g., Brander et al 2013;Biales et al 2015). However, a suite of bio-markers has not yet been identified to address ecosystem health questions in the Delta.…”