Similar flight performance but sex-specific mitochondrial responses in free-flying pigeons

Sex differences in metabolic responses of animals performing natural behaviours remain poorly understood, particularly under free-living conditions. Here, we examined how locomotor effort relates to mitochondrial metabolism in red blood cells in homing pigeons (Columba livia) by combining biologging of flight behaviour with measurements of mitochondrial respiration taken before and immediately after flight. Birds were equipped with global positioning system (GPS) loggers and tri-axial accelerometers, and movement effort was quantified using vectorial dynamic body acceleration (VeDBA). Flight was associated with a marked increase in mitochondrial respiration linked to aerobic energy production in both sexes, with increases ranging from 58.2% to 87.3% across traits. Males and females showed similar flight speeds, flight durations and social flight behaviour. Nevertheless, females showed higher VeDBA and higher post-flight mitochondrial aerobic metabolism than males, indicating sex differences in both mechanical and physiological responses. The relationship between VeDBA and post-flight mitochondrial metabolism was also sex-specific: as predicted, higher VeDBA was associated with higher ROUTINE and OXPHOS in males, but with lower values in females, a pattern for which we discuss possible physiological and behavioural explanations. Independent of flight status, males exhibited higher mitochondrial coupling efficiency than females, which was explained by their higher body mass. Together, these results provide evidence that flight effort was mirrored in blood mitochondrial metabolism and show that similar flight performance can mask potential sex-specific energetic signatures.