Abstract

Elevated summer river temperatures are associated with high in-river mortality in adult sockeye salmon (Oncorhynchus nerka) during their once-in-a-lifetime spawning migration up the Fraser River (British Columbia, Canada). However, the mechanisms underlying the decrease in whole-animal performance and cardiorespiratory collapse above optimal temperatures for aerobic scope (T opt) remain elusive for aquatic ectotherms. This is in part because all the relevant cardiorespiratory variables have rarely been measured directly and simultaneously during exercise at supra-optimal temperatures. Using the oxygen- and capacity-limited thermal tolerance hypothesis as a framework, this study simultaneously and directly measured oxygen consumption rate (MO2), cardiac output [Formula: see text], heart rate (f H), and cardiac stroke volume (V s), as well as arterial and venous blood oxygen status in adult sockeye salmon swimming at temperatures that bracketed T opt to elucidate possible limitations in oxygen uptake into the blood or internal delivery through the oxygen cascade. Above T opt, the decline in MO2max and aerobic scope was best explained by a cardiac limitation, triggered by reduced scope for f H. The highest test temperatures were characterized by a negative scope for f H, dramatic decreases in maximal [Formula: see text] and maximal V s, and cardiac dysrhythmias. In contrast, arterial blood oxygen content and partial pressure were almost insensitive to supra-optimal temperature, suggesting that oxygen delivery to and uptake by the gill were not a limiting factor. We propose that the high-temperature-induced en route mortality in migrating sockeye salmon may be at least partly attributed to physiological limitations in aerobic performance due to cardiac collapse via insufficient scope for f H. Furthermore, this improved mechanistic understanding of cardiorespiratory collapse at high temperature is likely to have broader application to other salmonids and perhaps other aquatic ectotherms.

Highlights

  • Temperature has been coined the ‘ecological master factor’ for ectotherms because of its influence on the biochemistry, physiology, behaviour, and ecology of animals (Fry, 1971)

  • This study overcame the difficult challenge of swimming a The results from the present study greatly expand upon the sufficient number of large fish equipped with cannulae and idea of a ‘death spiral’ for salmon swimming at ­supra-­optimal

  • venous partial pressure of oxygen (PvO2) (torr) Tmin[50–90] The optimal temperature (Topt) Tmax[50–90] Tmax[0–50] arterial oxygen content (CaO2) (ml dl−1) Tmin[50–90] Topt Tmax[50–90]

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Summary

Introduction

Temperature has been coined the ‘ecological master factor’ for ectotherms because of its influence on the biochemistry, physiology, behaviour, and ecology of animals (Fry, 1971). The Topt for aerobic scope has been established as a useful metric for the successful return of adult sockeye salmon to their natal spawning areas in the Fraser River watershed. Peak summer river ­temperatures have increased by around 2°C since the 1950s (Patterson et al, 2007), forcing salmon to migrate at temperatures warmer than their Topt for aerobic scope. There is great interest in the mechanism(s) underlying the decline of whole-animal performance and cardiorespiratory collapse above Topt

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