Abstract

Glucocorticoids are pleiotropic steroid hormones mediating redistribution of energy. They induce breakdown of glycogen stores and consequent plasma hyperglycaemia after stressful situations. Glucocorticoid actions in most vertebrate species are exerted by cortisol and corticosterone. However, 1α-hydroxycorticosterone is the dominant corticosteroid hormone in elasmobranchs, though its effects as a glucocorticoid are unknown. Here we demonstrate, by using ultra-performance liquid chromatography coupled to tandem mass spectrometry for the quantification of 1α-hydroxycorticosterone in plasma of the elasmobranch Scyliorhinus canicula, the response of this hormone to an acute-stress situation and for the first time its glucocorticoid action in elasmobranchs. After an acute air-exposure challenge, S. canicula increased plasma levels of 1α-hydroxycorticosterone altogether with enhanced glycolysis and gluconeogenesis pathways to fuel energy demanding tissues, such as white muscle, during the first hours after the stress situation. We foresee our study as a starting point to evaluate stress responses in elasmobranchs, as well as for future applications in the management of these key ecosystem species.

Highlights

  • The stress response in vertebrates has been studied in numerous species, whereby an immediate catecholamine mediated response is followed by a hypothalamic-pituitary-interrenal or -adrenal axis mediated release of glucocorticoids (Wendelaar Bonga, 1997; Sapolsky et al, 2000)

  • No mortality occurred during the experiment and all fish showed full physiological recovery within the first 24 h, coinciding with previous studies mimicking fisheries procedures and acute stress situations in other shark species (Cliff and Thurman, 1984; Richards et al, 2003; Kneebone et al, 2013)

  • The control group showed no changes in plasma 1α-hydroxycorticosterone at any of the sample points, while the levels in the stressed fish increased significantly after 18 min air exposure (0.47 ± 0.12 and 1.99 ± 1.05 nM for the control and air-exposed groups, respectively), reaching high values 5 h after recovery (7.33 ± 2.67 nM) (Figure 2)

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Summary

Introduction

The stress response in vertebrates has been studied in numerous species, whereby an immediate catecholamine mediated response is followed by a hypothalamic-pituitary-interrenal (in fish) or -adrenal (in other vertebrates) axis mediated release of glucocorticoids (Wendelaar Bonga, 1997; Sapolsky et al, 2000). Most studies on fish were performed on teleost fish, where differences have been described between taxa (Terrien and Prunet, 2013); data are limited for elasmobranchs where 1α-hydroxycorticosterone (1α-OH-B; 1α,11β,21-trihydroxy-4pregnene-3,20-dione), not cortisol, has been shown to be the dominant hormone (Idler and Kane, 1980) This corticosteroid was first isolated and characterized in 1966 (Idler and Truscott, 1966), and its mineralocorticoid activity has been described (Idler et al, 1967), mostly associated to the loss of plasma urea and sodium retention at lower environmental salinities in lesser spotted catshark (Scyliorhinus canicula) (Hazon and Henderson, 1984; Armour et al, 1993). Due to the difficulties in synthesizing this hormone (Anderson, 2012), the analytical methods used in the literature are based on other corticosteroids rather than 1α-hydroxycorticosterone (Evans et al, 2010; Brinn et al, 2012), rendering results less physiologically specific

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