Metabolic reduction after long duration flight is not related to fat-free mass loss or flight duration in a migratory passerine

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.

Long-duration wind tunnel flights reveal exponential declines in protein catabolism over time in short- and long-distance migratory warblers

“…To determine whether the environmental conditions influence fuel use, we flew birds overnight in minimal light conditions under both high evaporative water loss (HEWL; 2 g H2O m –3 ; 13% RH) and low evaporative water loss (LEWL; 12 g H2O m –3 ; 80% RH) conditions at 18 °C at 8 m/s wind speed. This wind speed was previously selected for yellow-rumped warblers to encourage flight in the wind tunnel and has been used for numerous experiments ( 17 , 40 , 44 , 45 ). For comparable measurements between the two warbler species, we also flew blackpoll warblers at the same speed.…”

“…Additional flight protocol details can be found in the study by Gerson et al. ( 17 ). Eighteen blackpoll warblers were selected for experiments, with nine flying in the wind tunnel at the facility and others serving as rest birds that were concurrently held in a covered cage in the plenum of the wind tunnel room to experience the same conditions alongside the flight.…”

“…( 22 ), including wing span (0.2108 m), wing area (0.0080 m 3 ), and flight muscle fraction of 0.156, which come from closely related Bay-breasted warblers ( Setophaga castanea ) and blackburnian warblers ( Setophaga fusca ) as reported in the study by Graber and Graber ( 51 ). We also used a BMR factor of 1.2 as this was the closest approximation of the preflight resting metabolic rate of yellow-rumped warblers from a previous wind tunnel study ( 17 ) and the fat-free mass-corrected estimate of the metabolic rate measured in our rest birds using QMR and DLW. The altitude of the simulations was set to 0 m above sea level to be comparable to the wind tunnel.…”

“…While the role of protein catabolism in migratory flight is not fully understood, it was long assumed that protein was spared as a fuel of last resort because it was documented as reductions to vital organs and muscles following nonstop flight ( 12 – 16 ). Therefore, the estimated ~5% of flight energy coming from protein may lead to functional losses that can impose important limits on flight duration and animal performance after flight ( 17 ).…”

“…Protein may also be a more responsive and beneficial fuel than previously acknowledged. For example, migratory white-throated sparrows ( Zonotrichia albicollis ) show a seasonal increase in the capacity to catabolize protein ( 28 ) and migratory songbirds flown in a wind tunnel show greater lean mass loss in response to drier conditions, indicating that lean mass may serve as a source for endogenous water during flight ( 17 , 29 , 30 ). Protein catabolism in migratory flight may also restore Krebs cycle intermediates that enable continued fatty acid catabolism ( 31 ), maintain optimal power to weight ratios as fuel loads change in flight ( 32 ), or reflect an imbalance between consistent, tissue-specific rates of protein catabolism and suppressed rates of protein synthesis ( 33 ).…”