Physiological Benefits of Being Small in a Changing World: Responses of Coho Salmon (Oncorhynchus kisutch) to an Acute Thermal Challenge and a Simulated Capture Event

Timothy D Clark,Andrew Lotto,David A Patterson,S Matthew Drenner,Scott G Hinch,Michael R Donaldson,Anthony P Farrell,Sebastian Pieperhoff,Steven J Cooke,Howard Browman

doi:10.1371/journal.pone.0039079

Abstract

Evidence is building to suggest that both chronic and acute warm temperature exposure, as well as other anthropogenic perturbations, may select for small adult fish within a species. To shed light on this phenomenon, we investigated physiological and anatomical attributes associated with size-specific responses to an acute thermal challenge and a fisheries capture simulation (exercise+air exposure) in maturing male coho salmon (Oncorhynchus kisutch). Full-size females were included for a sex-specific comparison. A size-specific response in haematology to an acute thermal challenge (from 7 to 20°C at 3°C h−1) was apparent only for plasma potassium, whereby full-size males exhibited a significant increase in comparison with smaller males (‘jacks’). Full-size females exhibited an elevated blood stress response in comparison with full-size males. Metabolic recovery following exhaustive exercise at 7°C was size-specific, with jacks regaining resting levels of metabolism at 9.3±0.5 h post-exercise in comparison with 12.3±0.4 h for full-size fish of both sexes. Excess post-exercise oxygen consumption scaled with body mass in male fish with an exponent of b = 1.20±0.08. Jacks appeared to regain osmoregulatory homeostasis faster than full-size males, and they had higher ventilation rates at 1 h post-exercise. Peak metabolic rate during post-exercise recovery scaled with body mass with an exponent of b∼1, suggesting that the slower metabolic recovery in large fish was not due to limitations in diffusive or convective oxygen transport, but that large fish simply accumulated a greater ‘oxygen debt’ that took longer to pay back at the size-independent peak metabolic rate of ∼6 mg min−1 kg−1. Post-exercise recovery of plasma testosterone was faster in jacks compared with full-size males, suggesting less impairment of the maturation trajectory of smaller fish. Supporting previous studies, these findings suggest that environmental change and non-lethal fisheries interactions have the potential to select for small individuals within fish populations over time.

Highlights

Evidence exists to suggest that both chronic and acute warm temperature exposure may benefit small animal species and small adult individuals within a species [1,2,3,4,5]
A negative correlation between the thermal environment and body size was first proposed over 160 years ago when Bergmann [6] documented this phenomenon for endothermic vertebrates over a large spatial scale
Climate change and variability are altering species distributions as populations respond to warming waters (e.g., [10]), and there is some correlative evidence to suggest intraspecific selection based on thermal interactions with body size [1,11]

Summary

Introduction

Evidence exists to suggest that both chronic and acute warm temperature exposure may benefit small animal species and small adult individuals within a species [1,2,3,4,5]. Climate change and variability are altering species distributions as populations respond to warming waters (e.g., [10]), and there is some correlative evidence to suggest intraspecific selection based on thermal interactions with body size [1,11]. Since the majority of information on the interaction between temperature tolerance and animal size stems from descriptive observations rather than controlled studies, contention surrounds the physiological mechanisms underlying the observed trends (e.g., see [8])

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Discussion

Conclusion