Flight muscle size reductions and functional changes following long-distance flight under variable humidity conditions in a migratory warbler

Abstract

Bird flight muscle can lose as much as 20% of its mass during a migratory flight due to protein catabolism, and catabolism can be further exacerbated under dehydrating conditions. However, the functional consequences of exercise and environment induced protein catabolism on muscle has not been examined. We hypothesized that prolonged flight would cause a decline in muscle mass, aerobic capacity, and contractile performance. This decline would be heightened for birds placed under dehydrating environmental conditions, which typically increases lean mass losses. Yellow-rumped warblers (Setophaga coronata) were exposed to dry or humid (12 or 80% relative humidity at 18°C) conditions for up to 6 h while at rest or undergoing flight. The pectoralis muscle was sampled after flight/rest or after 24 h of recovery, and contractile properties and enzymatic capacity for aerobic metabolism was measured. There was no change in lipid catabolism or force generation of the muscle due to flight or humidity, despite reductions in pectoralis dry mass immediately post-flight. However, there was a slowing of myosin-actin crossbridge kinetics under dry compared to humid conditions. Aerobic and contractile function is largely preserved after 6 h of exercise, suggesting that migratory birds preserve energy pathways and function in the muscle.

Keywords: atrophy; dehydration; exercise; migration; skeletal muscle.

FIGURE 1

The effect prolonged flight or rest under HEWL and LEWL conditions on the loss of (a) whole‐animal, (b) fat, and (c) nonfat mass. HEWL birds are represented by gray and LEWL in black. Flight birds are represented by circles and solid lines, and rest birds by triangles and dashed lines. There was a significant effect of flight treatment and duration in the wind tunnel on whole‐animal mass and fat mass. There was a significant effect of humidity and flight treatment on fat‐free mass loss. Sample sizes of each experimental group: Flight/HEWL/Recovery = 7; Flight/LEWL/Recovery = 6; Rest/HEWL/Recovery = 7, Rest/LEWL/Recovery = 6; Flight/HEWL/Post = 9; Flight/LEWL/Post = 10; Rest/HEWL/Post = 9; Rest/LEWL/Post = 10.

FIGURE 2

Difference in (a) whole‐animal, (b) fat mass, and (c) fat‐free mass between preexperimental and recovery of flight and rest birds, in relation to duration spent in the wind tunnel. There was a significant effect of duration in the wind tunnel and flight treatment on fat and whole‐animal mass. Humidity was not a significant factor. (sample size: Flight‐HEWL = 7; Flight‐LEWL = 6; Rest‐HEWL =. 7; Rest‐LEWL = 6).

FIGURE 3

Pectoralis (a) wet and (c) dry mass in relation to duration in the wind tunnel of flight and rest birds. Birds were either sampled immediately after experimental treatment or 24 h after the beginning of the experimental treatment. There was a significant interaction between flight treatment and duration in the wind tunnel on dry pectoralis mass. Pectoralis (b) wet and (d) dry mass of preflight controls were compared with experimental flight and rest birds with durations greater than 5 h. Humidity was not a significant factor and was subsequently removed in this latter analysis. *p < 0.05. (Sample sizes for figures A and C: Flight/HEWL/Recovery = 7; Flight/LEWL/Recovery = 6; Rest/HEWL/Recovery = 7, Rest/LEWL/Recovery = 5; Flight/HEWL/Post = 8; Flight/LEWL/Post = 9; Rest/HEWL/Post = 9; Rest/LEWL/Post = 8; Preflight control = 13. Sample sizes for figures B and D: Flight/Recovery = 6; Rest/Recovery = 5; Flight/Post = 13; Rest/Post = 14; Preflight control = 13. The number of males, females, and unknown are 38, 39, and 3, respectively, and both sexes were represented in all experimental groups).

FIGURE 4

Maximum enzyme activities (V_max) and protein content of the pectoralis major muscle from birds sampled preflight (control), immediately after exiting the wind tunnel (post) or 24 h of recovery (recovery). Humidity treatments are represented by dark gray or white for HEWL and LEWL, respectively. ALT: alanine aminotransferase; CPT, carnitine palmitoyl transferase; CS, citrate synthase; HOAD, 3‐hydroxyacyl CoA dehydrogenase; LDH, lactate dehydrogenase. * p < 0.05; ** p < 0.01. (Sample sizes of each experimental group: Flight/HEWL/Recovery = 7; Flight/LEWL/Recovery = 6; Rest/HEWL/Recovery = 7, Rest/LEWL/Recovery = 6; Flight/HEWL/Post = 9; Flight/LEWL/Post = 10; Rest/HEWL/Post = 9; Rest/LEWL/Post = 10; Preflight control = 16. The number of males, females, and unknown are 38, 39, and 3, respectively, and both sexes were represented in all experimental groups).

FIGURE 5

Single‐fiber contractile performance of the pectoralis muscle from yellow‐rumped warblers immediately following flight or rest treatment in HEWL and LEWL conditions. (a) Maximum force production at 25C, (b) muscle fiber cross‐sectional area, (c) apparent rate of myosin force production, and (d) mean myosin attachment time to Actin. * p < 0.05. There was a significant effect of humidity on mean myosin attachment time and a significant interaction between flight and humidity on 2πb.