In aerobic living systems, mitochondrial activity is the main physiological link between environmental resources or endogenous energy stores and energy allocated to animal performances. Mitochondrial oxidative phosphorylation is an energy transduction process coupling fuel oxidation and oxygen reduction (i.e. respiration) with the production of useable cellular energy in the form of ATP. The coupling ATP/O value (i.e. mitochondrial efficiency) is an important parameter of oxidative phosphorylation as it affects how much oxygen, and so how much nutrients, are needed to run such energy productive processes (Brand, 2005). In the present study, muscle mitochondrial efficiency was higher in fasted than in re-fed king penguin chicks, indicating that fasted chicks would consume fewer nutrients and oxygen to fuel their energy budgets. Such differences in the yield of mitochondrial ATP synthesis may be explained by intrinsic or extrinsic coupling mechanisms. The intrinsic mechanisms involve modifications in the properties of oxidative phosphorylation complexes, i.e. coupling stoichiometries H+ and O at the level of the respiratory chain or H+ and ATP at the level of ATP synthase (Brand, 2005). It has been observed that when such intrinsic mechanisms affect mitochondrial efficiency, then mitochondrial fluxes (oxygen consumption or ATP synthesis) are altered in association with modifications in the slope of the linear relation between oxygen consumption and ATP production (Rigoulet et al., 1990; Nogueira et al., 2002; Clerc et al., 2007; Salin et al., 2012). In the present study, oxygen consumption, ATP synthesis and slope values of linear relation between these two fluxes were not significantly different between fasted and re-fed chicks. These data would rule out a change in intrinsic coupling properties of the respiratory chain (H+/O) or the ATP synthase (H+/ATP) as a proximate mechanism of mitochondrial efficiency flexibility in winter-acclimatized chicks. The extrinsic mechanisms mainly involve proton leak reactions, which are processes that consume the proton motive force at the expense of ATP synthesis, and would greatly explain the non linear relationship between the effective ATP/O ratio and the oxygen consumption shown in Fig. 2C,D and Fig. 3C,D. Indeed, the non-ohmic nature of proton leak reactions implies that when mitochondrial phosphorylating activity increases, the flux through proton leak pathways greatly decreases, and the effective ATP/O ratio increases (Brand et al., 1993). At the maximal oxidative phosphorylation rate, leaks still occur, and the effective ATP/O ratio remains lower than the maximum possible value (Brand, 2005). If proton leak reactions are involved in the present increased ATP/O, we can predict from the literature a shift of the linear relationship between oxygen consumption and ATP synthesis to the left, with little effect on the slope and a significant decrease in basal non-phosphorylating respiration (Beavis and Lehninger, 1986; Clerc et al., 2007; Salin et al., 2010), which is clearly the case in the present study. In support of these data, one previous study has shown fatty acid and superoxide inducible mitochondrial proton leak activity to be decreased by 45% after a period of long-term caloric restriction in adult king penguins, an effect that was partly reversed by 3 days of re-feeding (Rey et al., 2008). Altogether, these data would suggest that skeletal muscle mitochondria are more energy efficient in long-term fasting chicks because a greater part of oxygen consumption and energy derived from nutrient oxidation is invested directly into ATP synthesis rather than dissipated as heat through proton leak reactions. By contrast, the fact that the apparent affinity of mitochondrial oxidation for ADP, which appears to be affected by proton leak rates (Gouspillou et al., 2011), did not differ between experimental groups would not support a difference in proton leak over the range of oxidative phosphorylation activity measured in the present study. However, we must keep in mind that the present study was not designed to accurately determine kinetic parameters of the oxidative phosphorylation (supplementary material Figs S1, S2). Hence, whether the higher mitochondrial oxidative phosphorylation efficiency of fasted winter chicks involves changes in proton leak reactions (e.g. membrane fatty acyl and phospholipids composition, and membrane protein activities, such as those of uncoupling protein and adenine nucleotide translocase) and/or in processes giving rise to a difference in membrane potential (e.g. citric acid cycle, electron transport chain) are currently not known but clearly warrant further investigations.