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Description
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Understanding how free-living animals meet the energetic demands of performing their everyday tasks is central to explaining how they cope with ecological challenges. Behavioral performance is often treated as a proxy for energetic expenditure, yet similar performance may arise from different physiological strategies. Such hidden variation may be particularly pronounced between sexes, which often differ in morphology, physiology, and energy allocation while performing similar activities. Yet sex differences in metabolic responses remain poorly understood in animals performing natural behaviors, particularly under free-living conditions. Here we examined how locomotor effort relates to mitochondrial metabolism in homing pigeons (Columba livia) by combining biologging of flight behavior with measurements of mitochondrial respiration in red blood cells taken before and immediately after flight. Birds were equipped with GPS loggers and tri-axial accelerometers. We quantified movement effort using Vectorial Dynamic Body Acceleration (VeDBA), a well-established index of energy expenditure. Overall, flight was associated with a marked increase in mitochondrial respiration linked to aerobic energy production, with increases ranging from 58.2% to 87.3% across traits, in both sexes. Flight performance did not differ between sexes: males and females showed similar flight speeds, flight durations, and social flight behavior (flying alone or in groups). Nevertheless, females, which are smaller than males, showed higher VeDBA and higher post-flight mitochondrial aerobic metabolism than males, indicating sex differences in both mechanical and physiological responses. Independently of flight status, males exhibited higher mitochondrial coupling efficiency than females, although this difference was accounted for by body mass, indicating that a greater proportion of respiration was used for ATP production rather than being dissipated as heat in heavier individuals. Together, these results show that similar flight performance can be associated with different energetic signatures and highlight sex as an important source of physiological variation in free-living animals.
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