Abstract

In female Atlantic salmon (Salmo salar), exposure to warm summer temperatures causes a reduction in plasma 17β-estradiol (E2), which impairs downstream vitellogenesis and zonagenesis, and reduces egg fertility and embryo survival. The aim of the present study was to determine whether E2-treatment could offset thermal impairment of endocrine function and maintain egg quality in maiden (first-time-spawning) S. salar reared at 22 °C. Treatment with E2 at 22 °C stimulated vitellogenin (vtg) gene expression and subsequent protein synthesis which promoted oocyte growth and increased egg size relative to untreated fish at 14 and 22 °C. However, E2-treatment at 22 °C was not associated with an increase in egg fertility and embryo survival relative to untreated fish at 22 °C, despite the positive effects of E2-treatment on vitellogenesis and oocyte growth. As there was no evidence to suggest that the estrogen receptor alpha expression was suppressed by high temperature, this could be due to the lack of stimulation on zonagenesis by E2-treatment observed at high temperature during oocyte development. Our results demonstrate that treatment with E2 is not able to maintain zonagenesis or egg quality in maiden S. salar at high temperature, even when vtg gene expression, protein synthesis and subsequent oocyte growth is promoted. This implies that the mechanisms regulating zonagenesis, but not vitellogenesis are impaired at elevated temperature in female S. salar broodstock, and highlights the remarkable complexity of thermally induced endocrine disruption in fish.

Highlights

  • Tasmanian Atlantic salmon (Salmo salar) are currently reared towards their upper-limit of thermal tolerance for successful reproduction (King & Pankhurst, 2003), and can sometimes experience temperatures up to and exceeding 20 ◦C during summer months (Battaglene et al, 2008)

  • Our results demonstrate that treatment with E2 is not able to maintain zonagenesis or egg quality in maiden S. salar at high temperature, even when vtg gene expression, protein synthesis and subsequent oocyte growth is promoted

  • Vtg uptake into the oocyte (Tyler, Sumpter & Bromage, 1988), and in the present study, E2-treated fish at 22 ◦C displayed higher levels of plasma Vtg than the control group at 22 ◦C at samples 2, 3 and 4. This difference was reflected by an increase in the rate of oocyte growth in E2-treated relative to untreated fish at elevated temperature. These results demonstrate that E2-treatment helped to maintain oocyte growth at 22 ◦C, and imply that the mechanisms governing Vtg uptake into developing oocytes are not impaired at high temperature in salmonids

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Summary

Introduction

Tasmanian Atlantic salmon (Salmo salar) are currently reared towards their upper-limit of thermal tolerance for successful reproduction (King & Pankhurst, 2003), and can sometimes experience temperatures up to and exceeding 20 ◦C during summer months (Battaglene et al, 2008). Endocrine impairment associated with exposure to elevated temperatures consistently leads to a reduction in egg fertility and embryo survival (King et al, 2003; Pankhurst et al, 1996; Taranger & Hansen, 1993), and the effects are typically more pronounced in maiden (first-time) spawning S. salar (Pankhurst et al, 2011). This indicates that the salmon industry must adapt to ensure the production of high quality smolts, as periods of high temperature become more frequent due to climate change (Pankhurst & King, 2010)

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