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).
Highlights
Endocrine disrupting chemicals (EDCs) agonize, antagonize or synergize the effects of endogenous hormones and are known to cause a number of physiological and behavioral abnormalities in fishes [1]
While the observed sex ratio in early spring ranged from 38–52% at the ranch beach in 2009 and 2010, respectively, the observed sex ratio at the urban beach ranged from 18–27%
While EDCs were detected at both sites via the CALUX assay and chemical analyses, responses in fish at the ranch site were limited to changes at the molecular level while putative impacts at numerous levels of biological organization were observed in samples from the urban site (Figure 12)
Summary
Endocrine disrupting chemicals (EDCs) agonize, antagonize or synergize the effects of endogenous hormones and are known to cause a number of physiological and behavioral abnormalities in fishes [1]. Examples of hormonal disruptions in fishes produced by EDCs include altered secondary sexual characteristics, males producing egg proteins (vitellogenin, choriogenin), and reduced sperm quality [5,6,7]. Both theoretical and empirical data indicate that EDCs can cause declines in fish populations [8,9]. To date no single study has attempted to link exposure to different environmental EDC mixtures, such as urban and ranch run-off, with responses at multiple tiers of the biological hierarchy, including population-level effects, within one study system. Linking molecular level responses (i.e. mRNA levels) with higher level effects (i.e. sex ratio) at sites exposed to different sources of EDCs may help to better determine the predictive value of biomarkers (i.e. vitellogenin)
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