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Songbirds meet the extreme metabolic demands of migration by burning both stored fat and protein. However, catabolizing these endogenous tissues for energy leads to organ atrophy, and reductions in gastrointestinal tissue can be as great as 50% of the pre-flight mass. Remarkably, during stopover refuelling birds quickly regain digestive mass and performance. Aminopep- tidase-N (APN) is a brush-border enzyme responsible for late-stage protein digestion and may critically assist tissue reconstruction during the stopover, thus compensating for reduced gut size. We hypothesized that birds recover- ing from a fast would differentially upregulate APN activity relative to disaccharidases to rapidly process and assimilate dietary protein into lean mass. We fasted 23 wild-caught migratory white-throated sparrows (Zonotrichia albicollis) for 48h to mimic mass reductions experienced during migratory flight and measured intestinal APN activity before the fast, immediately after the fast, and during recovery at 24 h and 48 h post- fast. Total fat mass, lean mass and basal metabolic rate were measured daily. We show that fasted birds maintain APN activity through the fast, despite a 30% reduction in intestine mass, but during refuelling, APN activity increases nearly twofold over pre-fasted individuals. This suggests that dynamically regulating APN may be necessary for rapid protein reconstruction during the stopover. 

ABSTRACT Migratory birds catabolize large quantities of protein during long flights, resulting in dramatic reductions in organ and muscle mass. One of the many hypotheses to explain this phenomenon is that decrease in lean mass is associated with reduced resting metabolism, saving energy after flight during refueling. However, the relationship between lean body mass and resting metabolic rate remains unclear. Furthermore, the coupling of lean mass with resting metabolic rate and with peak metabolic rate before and after long-duration flight have not previously been explored. We flew migratory yellow-rumped warblers ( Setophaga coronata ) in a wind tunnel under one of two humidity regimes to manipulate the rate of lean mass loss in flight, decoupling flight duration from total lean mass loss. Before and after long-duration flights, we measured resting and peak metabolism, and also measured fat mass and lean body mass using quantitative magnetic resonance. Flight duration ranged from 28 min to 600 min, and birds flying under dehydrating conditions lost more fat-free mass than those flying under humid conditions. After flight, there was a 14% reduction in resting metabolism but no change in peak metabolism. Interestingly, the reduction in resting metabolism was unrelated to flight duration or to change in fat-free body mass, indicating that protein metabolism in flight is unlikely to have evolved as an energy-saving measure to aid stopover refueling, but metabolic reduction itself is likely to be beneficial to migratory birds arriving in novel habitats. 

Migratory birds use protein as a fuel source during flight, but the mechanisms and benefits of protein catabolism during migration are poorly understood. The tissue-specific turnover rate hypothesis proposes that lean mass loss depends solely on the constitutive rate of protein degradation for a given tissue, and is therefore independent of metabolic rate or environmental stimuli. However, it has been demonstrated that environmental stressors such as humidity affect the rate of lean mass catabolism during flight, a finding that seemingly contradicts the tissue-specific turnover rate hypothesis. In order to resolve this, we placed migratory Swainson's thrushes in either high (HEWL) or low (LEWL) evaporative water loss conditions at rest and while undergoing simulated migratory flight at 8 m s−1 in a wind tunnel to test the impact of both environmental stressors and metabolic rate on the rate of protein breakdown. The total quantity and rate of lean mass loss was not different between flight and rest birds, but was affected by humidity condition, with HEWL losing significantly more lean mass. These results show that the rate of protein breakdown in migratory birds is independent of metabolic rate, but it can be augmented in response to environmental stressors.