Comparative responses to endocrine disrupting compounds in early life stages of Atlantic salmon, Salmo salar

Abstract

a b s t r a c tAtlantic salmon (Salmo salar) are endangered anadromous fish that may be exposed to feminizing endocrine disrupting compounds (EDCs) during early development, potentially altering physiological capacities, survival and fitness. To assess differential life stage sensitivity to common EDCs, we carried out short-term (4 day) exposures using three doses each of 17 ␣-ethinylestradiol (EE2), 17 ␤-estradiol (E2), and nonylphenol (NP) on four early life stages; embryos, yolk-sac larvae, feeding fry and 1 year old smolts. Differential response was compared using vitellogenin (Vtg, a precursor egg protein) gene transcription. Smolts were also examined for impacts on plasma Vtg, cortisol, thyroid hormones (T 4 /T 3 ) and hepatosomatic index (HSI). Compound-related mortality was not observed in any life stage, but Vtg mRNA was elevated in a dose-dependent manner in yolk-sac larvae, fry and smolts but not in embryos. The estrogens EE2 and E2 were consistently stronger inducers of Vtg than NP. Embryos responded significantly to the highest concentration of EE2 only, while older life stages responded to the highest doses of all three compounds, as well as intermediate doses of EE2 and E2. Maximal transcription was greater for fry among the three earliest life stages, suggesting fry may be the most responsive life stage in early development. Smolt plasma Vtg was also significantly increased, and this response was observed at lower doses of each compound than was detected by gene transcription suggesting plasma Vtg is a more sensitive indicator at this life stage. HSI was increased at the highest doses of EE2 and E2, and plasma T 3 was decreased at the highest dose of EE2. Our results indicate that all life stages are potentially sensitive to endocrine disruption by estrogenic compounds and that physiological responses were altered over a short window of exposure, indicating the potential for these compounds to impact fish in the wild.

2, 4-Dichloro-6-nitrophenol, a photonitration product of 2, 4-dichlorophenol, caused anti-androgenic potency in Chinese rare minnows (Gobiocypris rarus)

“…Regarding the sex steroid levels, the endocrine system in males and juvenile fish was more affected than that in females. Similar observations concerning differential life stage sensitivity have been reported in other studies (Duffy et al, 2014;Liney et al, 2005). Moreover, antiandrogenic effects may be provoked by inhibition of testosterone synthesis.…”

“…In addition, in vivo studies have indicated that substituted phenols can alter the expression of the steroid receptors associated with changes in the metabolism of xenobiotics and steroid hormones (Zhang et al, 2008). Therefore, potent estrogenic effects of substituted phenols (e.g., Nonylphenol and Tribromophenol) have been found in vitro (Bonefeld-Jorgensen et al, 2007) and in vivo (Deng et al, 2010;Duffy et al, 2014). However, the impact on the endocrine system is not the same as that of natural hormones because the estrogenic effects of substituted phenols are weak.…”

Low adaptive potential for tolerance to ethynylestradiol, but also low toxicity, in a grayling population (Thymallus thymallus)

“…Atlantic salmon [37,38] but was not observed in brown trout [11]. One possible explanation for this apparent discrepancy between brown trout and grayling larvae is that hatching was not induced in the study on brown trout [11] but induced by an increase in temperature in the present study on grayling.…”

“…Akaike's information criteria (AIC) were used as measures of model fit and model complexity, and likelihood ratio tests (LRT) were used to compare models. All the mixed-effects models were fitted with the lme4 R package[36] and all the statistical analyses were performed in R[37].…”

Low adaptive potential for tolerance to ethynylestradiol, but also low toxicity, in a grayling population (Thymallus thymallus)

“…Marques da Cunha et al [11] found EE2 to reduce embryo survival by only 0.9 percent points, and they found no additive genetic variance for the tolerance to EE2 in seven genetically distinct populations. Duffy et al [23] found no EE2-induced mortality in embryos and larvae of Atlantic salmon. They also studied vitellogenin gene transcription and plasma concentrations and found this precursor egg protein to be significantly affected only in embryos exposed to EE2 concentrations that may be too high to be ecologically relevant.…”