Depletion of Essential Fatty Acids in the Food Source Affects Aerobic Capacities of the Golden Grey Mullet Liza aurata in a Warming Seawater Context.

Marie Vagner,Thomas Lacoue-Labarthe,Christel Lefrançois,David Mazurais,Hervé Le Delliou,Emmanuel Dubillot,Patrick Quazuguel,José-Luis Zambonino Infante,Daniel E Crocker

doi:10.1371/journal.pone.0126489

Marie Vagner, Thomas Lacoue-Labarthe + Show 7 more

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https://doi.org/10.1371/journal.pone.0126489

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Abstract

The objective of this study was to evaluate the combined effects of thermal acclimation and n-3 highly unsaturated fatty acids (n-3 HUFA) content of the food source on the aerobic capacities of fish in a thermal changing environment. The model used was the golden grey mullet Liza aurata, a species of high ecological importance in temperate coastal areas. For four months, fish were exposed to two food sources with contrasting n-3 HUFA contents (4.8% ecosapentaenoic acid EPA + docosahexaenoic acid DHA on the dry matter DM basis vs. 0.2% EPA+DHA on DM) combined with two acclimation temperatures (12°C vs. 20°C). The four experimental conditions were LH12, LH20, HH12 and HH20. Each group was then submitted to a thermal challenge consisting of successive exposures to five temperatures (9°C, 12°C, 16°C, 20°C, 24°C). At each temperature, the maximal and minimal metabolic rates, metabolic scope, and the maximum swimming speed were measured. Results showed that the cost of maintenance of basal metabolic activities was particularly higher when n-3 HUFA food content was low. Moreover, fish exposed to high acclimation temperature combined with a low n-3 HUFA dietary level (LH20) exhibited a higher aerobic scope, as well as a greater expenditure of energy to reach the same maximum swimming speed as other groups. This suggested a reduction of the amount of energy available to perform other physiological functions. This study is the first to show that the impact of lowering n-3 HUFA food content is exacerbated for fish previously acclimated to a warmer environment. It raises the question of the consequences of longer and warmer summers that have already been recorded and are still expected in temperate areas, as well as the pertinence of the lowering n-3 HUFA availability in the food web expected with global change, as a factor affecting marine organisms and communities.

Highlights

Thermal tolerance varies widely among species and has been shown to be dependent on the acclimation temperature [1], as well as on the physiological plasticity of organisms [2]
Regarding the initial fish composition, and as expected, the high HUFA diet (HH) diet induced an increase in n-3 HUFA and S n-3 fatty acid (FA) in fish PL, while the low-n-3 HUFA diet (LH) diet induced a depletion in these FA contents, but an increase in n-6 FA instead
EPA and the ratio n-3/n-6 FA contents were significantly affected by an interaction between acclimation temperature and diet, and EPA was less incorporated in PL and NL of LH20 fish

Summary

Introduction

Thermal tolerance varies widely among species and has been shown to be dependent on the acclimation temperature [1], as well as on the physiological plasticity of organisms [2]. When exposed to environmental temperature changes, ectotherms rapidly modulate the phospholipid composition of their cell membranes in terms of highly unsaturated fatty acids of the n-3 series (n-3 HUFA) in order to maintain their physiological performances [3,4] This adjustment of the rate of n-3 HUFA in cell membrane determines the degree of unsaturation of the phospholipid and is necessary for maintaining membrane fluidity, and the membrane functionality in a thermal changing environment [3]. When the membrane fluidity tends to decrease at low temperatures, the degree of lipid unsaturation tends to increase to maintain its properties and functionality [5], and vice versa when the temperature increases [6] These lipid adjustments in cell membranes can maintain the activity of transmembrane proteins [7,8], and are determinant for the maintenance of numerous physiological functions (for review see [9,10,11]). These fatty acids have been shown to be essential for growth, survival, pigmentation, development and functionality of the brain, vision, and nervous system, as well as in resistance to stress and disease, as they are precursors of eicosanoids (for reviews see [9,11])

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