Abstract
Many migrating birds undertake extraordinary long flights. How birds are able to perform such endurance flights of over 100-hour durations is still poorly understood. We examined energy expenditure and physiological changes in Northern Bald Ibis Geronticus eremite during natural flights using birds trained to follow an ultra-light aircraft. Because these birds were tame, with foster parents, we were able to bleed them immediately prior to and after each flight. Flight duration was experimentally designed ranging between one and almost four hours continuous flights. Energy expenditure during flight was estimated using doubly-labelled-water while physiological properties were assessed through blood chemistry including plasma metabolites, enzymes, electrolytes, blood gases, and reactive oxygen compounds. Instantaneous energy expenditure decreased with flight duration, and the birds appeared to balance aerobic and anaerobic metabolism, using fat, carbohydrate and protein as fuel. This made flight both economic and tolerable. The observed effects resemble classical exercise adaptations that can limit duration of exercise while reducing energetic output. There were also in-flight benefits that enable power output variation from cruising to manoeuvring. These adaptations share characteristics with physiological processes that have facilitated other athletic feats in nature and might enable the extraordinary long flights of migratory birds as well.
Highlights
Nonstop flapping flights across large geographic barriers such as deserts or oceans during migration [1,2,3] are extreme and fascinating achievements, but the physiological adaptationsPLOS ONE | DOI:10.1371/journal.pone.0134433 September 16, 2015Ibis Flight associated with these feats are not thoroughly understood
Flight energy expenditure was significantly elevated above non-flight energy expenditure (Fig 1A; paired t-test: t41 = 12.307, p
As flight durations were distributed over the season, and as energy expenditure did not correlate with calendar date training was not a factor in energy expenditure
Summary
Nonstop flapping flights across large geographic barriers such as deserts or oceans during migration [1,2,3] are extreme and fascinating achievements, but the physiological adaptationsPLOS ONE | DOI:10.1371/journal.pone.0134433 September 16, 2015Ibis Flight associated with these feats are not thoroughly understood. The availability of fuel along with a variety of other factors may change flight performance and could limit endurance These other factors include the accumulation of lactate and oxidative damage, dehydration, electrolyte imbalance and acidosis, glycogen depletion, exceeding capacities for fat and protein catabolism, and oxygen debt. Following the typical mammalian model of exercise, one would expect flight to be accompanied by similar cost accumulations, fuel depletion, increased energy expenditure and exhaustion. This view is partly supported by studies on migrating birds but has become difficult to generalize in light of documented extremes in migratory performance, like the eight-day trans-Pacific flight of a Godwit [1], or the 3400 km trans-Atlantic flight of a Northern Wheatear [3]
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