Metabolic responses of homing pigeons to flight and subsequent recovery

Abstract

This study examines metabolic changes occurring during short to endurance flights and during subsequent recovery in free-flying pigeons, in particular the change towards lipid utilization with increasing flight duration, lipid supply to the flight muscles, protein utilization and the time needed to metabolically recover. Eight plasma metabolite concentrations were measured in homing pigeons released from sites 20–200 km from the loft (0.3–4.8 h flight duration) just after landing and after keeping birds fasting at rest for 30 and 60 min, respectively, after their return. Birds kept in the loft fasting at rest were used as controls. Plasma free fatty acid and glycerol concentrations increased rapidly with flight duration and leveled off after about 1.5 h. This indicates a marked change towards a high and stable lipid utilization from adipose tissues within 1–2 h of flight. Plasma triglyceride levels and very-low-density lipoproteins were decreased after short flights, but subsequently regained or surpassed fasting levels at rest. This indicates that re-esterification of free fatty acids and delivery as very-low-density lipoproteins to the flight muscles to circumvent constraints of fatty acid supply, as described previously for small passerines, is not as significant in the pigeon which has a much lower mass-specific energy rate. An initial increase in plasma glucose levels and a transient decrease to fasting levels at rest was observed and may reflect the initial use and subsequent exhaustion of glycogen stores. Contrary to other birds and mammals, β-hydroxy-butyrate levels increased markedly with flight duration. This may suggest a more important sparing of carbohydrates and protein as gluconeogenic precursors in the pigeon than in other species. Plasma uric acid levels increased linearly up to about 4 h flight duration. This indicates an accelerated protein breakdown during flight which may primarily serve to deliver amino acids as glucogenic precursors and citrate cycle intermediates. With increasing flight duration, the energy sources change from an initial phase based primarily on carbohydrates to a lipid-based endurance phase. It is discussed whether this metabolic change depends on the level of power output or the performed work (energy spent) since the start of flight. During the first hour of recovery, most metabolites reached or approached fasting levels at rest, indicating a marked reduction in lipolysis and protein breakdown. β-hydroxy-butyrate levels remained at flight levels and glucose levels increased slightly, indicating a restoration of glycogen stores.