Plasma 1α-Hydroxycorticosterone as Biomarker for Acute Stress in Catsharks (Scyliorhinus canicula)

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.

Physiology: An Important Tool to Assess the Welfare of Aquatic Animals

“…The physiological recovery of sharks is involved in the improvement of the survival rates after catch-and-release [ 60 ]. Recent advances in elasmobranch physiology highlight the release of catecholamines (adrenaline and noradrenaline) and corticosteroids (1α-hydroxycorticosterone) into the bloodstream as primary stress responses [ 53 , 100 ]. Secondary stress responses include changes in circulating ion concentrations [ 101 ], pH, and urea as the main metabolite controlling plasma osmolality levels in marine elasmobranchs [ 60 , 102 ].…”

“…Secondary stress responses include changes in circulating ion concentrations [ 101 ], pH, and urea as the main metabolite controlling plasma osmolality levels in marine elasmobranchs [ 60 , 102 ]. While amino acids are conspicuously of paramount importance as oxidative substrates in white muscle of this taxa [ 103 ], carbohydrates have been shown to be relevant energy substrates after acute stress challenges [ 53 ]. The analysis of certain blood parameters seems to offer a picture of the physiological status of elasmobranchs at a certain moment, highlighting plasma pH, glucose, lactate, and K + levels as selected biomarkers.…”

“…The analysis of certain blood parameters seems to offer a picture of the physiological status of elasmobranchs at a certain moment, highlighting plasma pH, glucose, lactate, and K + levels as selected biomarkers. However, large differences are described depending on the species [ 53 , 60 , 68 , 99 , 104 ], so that further studies are needed to better describe short- and long-term stress responses of these animals and their relationship to elasmobranch welfare.…”

“…CNS (Central Nervous System). This figure is based on information from several sources, including [ 31 , 50 , 53 , 57 , 58 , 59 , 60 ].…”

“…After integrating a stressor, the animal processes the information through its nervous system and alerts the body. The first responses include the secretion to the circulatory system of neuroendocrine hormones such as catecholamines [ 51 , 52 ] and others, including corticosteroids in vertebrates [ 21 , 53 , 54 ] and hyperglycemic hormone in crustaceans [ 55 ]. These hormones induce secondary stress responses, increasing heart and respiration frequency rates, and mobilizing energy metabolites to cover the demand for energy and oxygen imposed by the stressor [ 21 , 31 , 56 , 57 , 58 ].…”