Lipid-induced thermogenesis is up-regulated by the first cold-water immersions in juvenile penguins

Abstract

The passage from shore to marine life is a critical step in the development of juvenile penguins and is characterized by a fuel selection towards lipid oxidation concomitant to an enhancement of lipid-induced thermogenesis. However, mechanisms of such thermogenic improvement at fledging remain undefined. We used two different groups of pre-fledging king penguins (Aptenodytes patagonicus) to investigate the specific contribution of cold exposure during water immersion to lipid metabolism. Terrestrial penguins that had never been immersed in cold water were compared with experimentally cold-water immersed juveniles. Experimentally immersed penguins underwent ten successive immersions at approximately 9-10 °C for 5 h over 3 weeks. We evaluated adaptive thermogenesis by measuring body temperature, metabolic rate and shivering activity in fully immersed penguins exposed to water temperatures ranging from 12 to 29 °C. Both never-immersed and experimentally immersed penguins were able to maintain their homeothermy in cold water, exhibiting similar thermogenic activity. In vivo, perfusion of lipid emulsion at thermoneutrality induced a twofold larger calorigenic response in experimentally immersed than in never-immersed birds. In vitro, the respiratory rates and the oxidative phosphorylation efficiency of isolated muscle mitochondria were not improved with cold-water immersions. The present study shows that acclimation to cold water only partially reproduced the fuel selection towards lipid oxidation that characterizes penguin acclimatization to marine life.

Skeletal muscle metabolism in sea-acclimatized king penguins: I. Thermogenic mechanisms

“…Thus, both groups exhibited the same thermal sensitivity to cold water, increasing their metabolic heat production when exposed to the same lower critical water temperature of 26-27°C or less. Such high temperatures of the lower limit of the thermoneutral zone in water have previously been reported in several penguin species (Kooyman et al, 1976;Barré and Roussel, 1986;Dumonteil et al, 1994;Teulier et al, 2016). These results clearly indicate that at the time of their first departure out to sea, juveniles are already equipped to be effective endotherms in cold water.…”

“…This is supported by the fact that (i) cold-deacclimatized juveniles, i.e. juveniles kept for 2 weeks at 20°C, are less efficient thermoregulators during cold immersion than sea-acclimatized penguins (Barré and Roussel, 1986); and (ii) 10 successive immersions in cold water can improve the thermoregulatory capacity of cold-deacclimatized juveniles (Barré and Roussel, 1986) but not of juveniles kept outside in their natural environment (Teulier et al, 2016), which in turn exhibit the same thermoregulatory capacity as sea-acclimatized immatures ( present study). Fig.…”

“…At sea, heat losses and the daily metabolic costs of thermoregulation are reduced by penguins' ability to develop powerful peripheral vasoconstriction, regional hypothermia and a thick layer of subcutaneous fat (Dumonteil et al, 1994;Handrich et al, 1997;Lewden et al, 2017a;Enstipp et al, 2017). However, acute immersion in cold water induces up to a threefold increase in penguin resting metabolic rate (Barré and Roussel, 1986;Stahel and Nicol, 1988;Kooyman et al, 1992;Culik et al, 1996;Fahlman et al, 2004Fahlman et al, , 2005Rey et al, 2016), while repeated immersions of juveniles in cold water or sea acclimatization trigger an increase in their thermogenic capacity (Barré and Roussel, 1986;Teulier et al, 2012Teulier et al, , 2016Rey et al, 2016). Hence, the survival of penguins in cold water also depends on their ability to sustain high levels of energy expenditure and heat production over long periods.…”

Apparent changes in body insulation of juvenile king penguins suggest an energetic challenge during their early life at sea

“…5). Previous studies showed that the thermogenic capacity of juvenile king penguins increases after repeated experimental submersion in cold water (Barré and Roussel, 1986;Talbot et al, 2004;Teulier et al, 2016) and is considerably higher in immature birds (after ∼1 year at sea) than in juveniles before their first departure to sea (Teulier et al, 2012). Hence, the relatively high peripheral temperatures during diving that we observed in juveniles during their initial period at sea could potentially also be a consequence of insufficient thermogenic capacity, so that birds avoid a deeper temperature drop by maintaining some peripheral perfusion.…”

Chronic cold exposure induces mitochondrial plasticity in deer mice native to high altitudes

“…2004; Teulier et al . 2016). In both cases, increases in flux through pathways of mitochondrial energy metabolism – either to support ATP synthesis or to counteract proton leak – is an important source of heat production.…”