Energy conservation is a key priority for organisms living in environments with seasonal or unpredictable shortages in resource supplies. This is exemplified in hibernating or aestivating animals that undergo long periods of torpor (Geiser, 2004). However, previous studies have shown that energy conservation in animals undergoing dormancy is mainly achieved by an overall metabolic depression in conjunction with a reduction in mitochondrial oxidative phosphorylation activity rather than a downregulation of mitochondrial coupling efficiency (Staples and Brown, 2008). As commonly reported in food-restricted birds (Walker et al., 1983; McKechnie and Lovegrove, 2002), king penguin chicks experience shallow hypothermia, resulting in progressive body temperature decline throughout the winter fast that can fall as low as 30–33°C in the deep core of a chick's body near to the heart and the liver (Eichhorn et al., 2011). Even though those authors did not report a temperature for pectoral muscle, the fact that the thermal gradient between the deep core and the body shell can be as large as 8–15°C would indicate that pectoral muscles undergo a physiological hypothermia, at least similar to that measured in the thorax and the upper abdominal site near to the liver, i.e. down to 30–33°C (Eichhorn et al., 2011). Here, we show that such a level of heterothermy induced a significant 23% increase in the energy coupling efficiency at the level of mitochondria with an overall decrease in mitochondrial oxidative activity. Furthermore, we found coupling efficiency to be increased in conjunction with decreased basal non-phosphorylating oxygen consumption and oxidative activity. It is now well known that the effect of temperature on basal mitochondrial respiration reflects that on mitochondrial proton leak activities (Dufour et al., 1996; Chamberlin, 2004; Keller et al., 2004; Brown et al., 2007; Brown et al., 2012). In addition, in the high temperature range used in the present study, the inner membrane potential would be unaffected (Dufour et al., 1996; Chamberlin, 2004) and the occurrence of intrinsic coupling mechanisms, i.e. stoichiometry of oxidative phosphorylation complexes, negligible (Canton et al., 1995; Brand et al., 1994). In light of these studies, we interpret our findings as evidence that hypothermic mitochondria operate with higher efficiency because the lower oxidative activity (e.g. lower production of mitochondrial membrane potential) would be compensated for by a decrease in inner membrane proton leak rate (e.g. lower consumption of mitochondrial membrane potential), resulting in homeostasis of the proton motive force, and thus the flux of ATP synthesis would remain stable. Notwithstanding the underlying mechanisms, the present results clearly indicate that king penguin chicks realize additional energy savings while becoming hypothermic during winter.