Abstract

AbstractOmega‐3 long‐chain polyunsaturated fatty acids (n − 3 LC‐PUFA) are essential micronutrients for optimal functioning of cellular metabolism and for somatic growth of all vertebrates including fishes. In addition,n − 3 LC‐PUFA could also play a key role in response of fishes and other ectothermic vertebrates to changing temperatures.An important, but largely overlooked, consequence of climate change is the reduced availability of dietaryn − 3 LC‐PUFA in aquatic food webs. Changes in availability of dietaryn − 3 LC‐PUFA have recently been proposed as a major driver of novel adaptations and diversification of consumers. Yet, there is only limited knowledge about hown − 3 LC‐PUFA depletion in aquatic food webs will affect the performance of wild fishes.Here we combine biochemistry and physiology at the cellular level with physiological and cognitive processes at the whole‐animal level to test how ecologically relevant deprivation ofn − 3 LC‐PUFA affects performance of wild juvenile Atlantic salmonSalmo salar.We found that juvenile salmon had a limited capacity to maintain the fatty acid profile of both muscle and brain under ann − 3 LC‐PUFA‐deficient diet. Despite these findings, brain tissues showed remarkable functional stability in mitochondrial metabolism, and we found no effect of diet on learning ability. However, we found that mitochondrial efficiency in muscles and the somatic growth were reduced under ann − 3 LC‐PUFA‐deficient diet. Importantly, we discovered that the somatic growth of juvenile salmon within both treatments decreased with increasing rate of DHA synthesis and retention.Since DHA is essential for functioning of cellular metabolism, which together with body size are traits closely related to fitness of wild fishes, we suggest that the trade‐off between growth rate and accumulation of DHA could play a critical role in resilience of juvenile salmon to the ongoing rapid environmental change.A freePlain Language Summarycan be found within the Supporting Information of this article.

Highlights

  • An important but poorly understood consequence of climate change is the reduced availability of omega-­3 long-­chain polyunsaturated fatty acids (n − 3 LC-­PUFA), eicosapentaenoic acid (EPA, 20:5 n − 3) and docosahexaenoic acid (DHA, 22:6 n − 3), in aquatic food webs (Fuiman, 2018; Hixson & Arts, 2016; Taipale et al, 2018)

  • Our results show that dietary deprivation of n − 3 LC-­PUFA induced by experimental treatment simulating subsidies from a degraded aquatic food web caused, in comparison to a control diet, a change in the fatty acid composition and, importantly, a decrease of DHA content in the muscle and brain of juvenile salmon

  • The reduced tissue content of DHA coincided with reduced mitochondrial efficiency of ATP production in muscle, but it did not affect maximum metabolic rate

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Summary

| INTRODUCTION

An important but poorly understood consequence of climate change is the reduced availability of omega-­3 long-­chain polyunsaturated fatty acids (n − 3 LC-­PUFA), eicosapentaenoic acid (EPA, 20:5 n − 3) and docosahexaenoic acid (DHA, 22:6 n − 3), in aquatic food webs (Fuiman, 2018; Hixson & Arts, 2016; Taipale et al, 2018) This issue is especially pressing in temperate headwater streams vulnerable to rapid decrease of these micronutrients because increasing temperature (Hixson & Arts, 2016) and frequency of extreme weather events, such as torrential rains (Kanno et al, 2014; Woodward et al, 2015). Our experimental design allowed us to test whether an n − 3 LC-­PUFA-­deprived diet: (a) leads to a reduction of n − 3 LC-­PUFA and DHA in brain and muscle tissues; (b) decreases efficiency of mitochondrial metabolism and increases maximum metabolic rate (MMR) at elevated temperature; (c) reduces brain size and deteriorates learning ability at elevated temperature and (d) has a negative effect on somatic growth of wild fish

| MATERIALS AND METHODS
Findings
| DISCUSSION
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