Large muscles are beneficial but not required for improving thermogenic capacity in small birds

Myriam S Milbergue,Pierre U Blier,François Vézina

doi:10.1038/s41598-018-32041-w

Myriam S Milbergue, Pierre U Blier + Show 1 more

Open Access

https://doi.org/10.1038/s41598-018-32041-w

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Abstract

It is generally assumed that small birds improve their shivering heat production capacity by developing the size of their pectoralis muscles. However, some studies have reported an enhancement of thermogenic capacity in the absence of muscle mass variation between seasons or thermal treatments. We tested the hypothesis that an increase in muscle mass is not a prerequisite for improving avian thermogenic capacity. We measured basal (BMR) and summit (Msum) metabolic rates of black capped chickadees (Poecile atricapillus) acclimated to thermoneutral (27 °C) and cold (−10 °C) temperatures and obtained body composition data from dissections. Cold acclimated birds consumed 44% more food, and had 5% and 20% higher BMR and Msum, respectively, compared to individuals kept at thermoneutrality. However, lean dry pectoralis and total muscle mass did not differ between treatments, confirming that the improvement of thermogenic capacity did not require an increase in skeletal muscle mass. Nevertheless, within temperature treatments, Msum was positively correlated with the mass of all measured muscles, including the pectoralis. Therefore, for a given acclimation temperature individuals with large muscles do benefit from muscle size in term of heat production but improving thermogenic capacity during cold acclimation likely requires an upregulation of cell functions.

Highlights

For small avian species wintering at high latitudes, winter acclimatization is mainly a physiological phenomenon1–5 where cold hardiness is improved as temperature decline from fall to peak of winter5–8
We expected higher thermogenic capacity in cold-acclimated birds relative to individuals kept at thermoneutrality and predicted that this difference would not result from larger skeletal muscles in the cold
Our data support this hypothesis as cold-acclimated individuals had a measured basal (BMR) and summit (Msum) 20% higher but had smaller leg muscles and did not develop larger pectoralis, carcass or total muscles than birds kept at 27 °C

Summary

Introduction

For small avian species wintering at high latitudes, winter acclimatization is mainly a physiological phenomenon where cold hardiness is improved as temperature decline from fall to peak of winter. Despite the seasonal changes in muscles size and Msum observed in the wild, a small number of studies, they were not designed to investigate this specific phenomenon, reported improvements of thermogenic capacity in controlled conditions independently from changes in muscles size. Despite the seasonal changes in muscles size and Msum observed in the wild, a small number of studies, they were not designed to investigate this specific phenomenon, reported improvements of thermogenic capacity in controlled conditions independently from changes in muscles size19,38,39 This phenomenon was found to occur even in species known to increase pectoralis muscle mass in winter. In this particular case, the expected positive correlation between heart and muscles mass and Msum was found in cold acclimated birds, there was no significant difference in the mass of pectoralis or other skeletal muscles between thermal treatments. The experimental evidence presented above suggest that developing larger muscles may not be an obligate prerequisite for improving individual thermogenic capacity, even in species known to increase the size of their muscles during cold winters

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