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Thesis Format

Integrated Article

Degree

Doctor of Philosophy

Program

Biology

Supervisor

Staples, James F

2nd Supervisor

Guglielmo, Christopher G

Joint Supervisor

Abstract

Migratory birds make large-scale movements using flight twice per year, which are physiologically challenging due to high energetic costs and oxidative damage from reactive oxygen species (ROS). Muscle mitochondria play central roles in energy supply and ROS homeostasis during exercise, but the role of mitochondrial function in overcoming the demands of migratory flight is presently unclear. In this dissertation, I explore how mitochondrial function is modulated in three contexts relevant to avian migration: seasonal flexibility, endurance flight and evolved variation in migration strategy. For my first aim, I compared flight muscle mitochondrial respiration and ROS emission between a migratory and short-day photoperiod-induced non-migratory phenotype in yellow-rumped warblers (Setophaga coronata). I found that fatty acid-fuelled respiration was higher and ROS emission was lower in the migratory compared to the non-migratory phenotype, indicating that mitochondria are seasonally remodeled to support greater fatty acid oxidation and lower risk of oxidative stress during migration. For my second aim, I assessed mitochondrial respiration and ROS emission and lean tissue catabolism before and after up to eight hour endurance flight using a wind tunnel in blackpoll warblers (Setophaga striata). I found that endurance flight had little effect on flight muscle size, ultrastructure, mitochondrial respiration or ROS emission, but a modest reduction in the mass of liver, gizzard and proventriculus. These findings suggest that mitochondria are resilient against the damaging aspects of endurance flight and that the flight muscle may be preferentially protected to support endurance flight performance. For my third aim, I assessed pectoralis size, mitochondrial physiology, and mitochondrial abundance across 19 passerine species of varying migratory strategy. I found that long-distance migration was associated with lower pectoralis size and fatty acid oxidation capacity, while mitochondrial abundance and ROS emission were unaffected. Surprisingly, these data suggest that longer migration distance is associated with a lower oxidative capacity, which may reflect evolved reductions in energy expenditure during migration. Together, my findings indicate that mitochondrial metabolism is modulated by migratory songbirds to better meet the demands of migratory flight.

Summary for Lay Audience

Migratory birds make some of the largest scale movements in nature, but how they accomplish these feats of endurance exercise is poorly understood. One way that migratory birds can facilitate these movements is by changing the function of structures within their muscles called mitochondria, which supply the energy used during exercise, but can produce potentially harmful chemicals called reactive oxygen species (ROS). In my thesis, I investigated the role of mitochondria in bird migration by comparing mitochondrial function across three different aspects of migration: 1) during and after migratory season, 2) before and immediately after extended flights using a wind tunnel and 3) comparing between species that migrate different distances. For all studies, I measured how quickly flight muscle mitochondria consumed oxygen and produced ROS when burning fat as a fuel. I found that in the migratory season, mitochondria consume more oxygen and produce less ROS compared to after migration, suggesting that migratory birds modify their mitochondria to increase energy supply and lower the risk of damage during flight. Next, I found that eight hour wind tunnel flight had no effect on mitochondrial oxygen consumption or ROS production, indicating that mitochondria are not damaged during flight. Finally, I found that long-distance migratory species had lower oxygen consumption, similar ROS production and smaller flight muscles compared to short-distance migrants. This surprising finding suggests that long-distance migrants (which are assumed to have the most difficult migrations) have flight muscles that have a lower capacity for exercise, which indicates that long-distance migrants use energy-efficient flight. The results of my studies show that mitochondrial function is dynamic with respect to migration in birds. These findings improve our understanding of how muscle metabolism can be changed to better meet the demands of endurance exercise.

Creative Commons License

Creative Commons Attribution-Noncommercial 4.0 License
This work is licensed under a Creative Commons Attribution-Noncommercial 4.0 License

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