Nonshivering thermogenesis and adaptation to fasting in king penguin chicks

Abstract

The ability to develop nonshivering thermogenesis (NST) and the effect of fasting on thermogenic response to cold were studied in winter-acclimatized king penguin chicks. Metabolic rate (MR) and integrated electrical muscle activity were measured at different ambient temperatures. In cold-acclimatized (5 degrees C) fed chicks, shivering threshold temperature (STT) was 9.4 degrees C lower than lower critical temperature (LCT), indicating that NST (0.7 W/kg) occurs at moderate cold, whereas in control chicks fed and reared at 25 degrees C for 3 wk, LCT and STT were similar. Chicks reared in the cold and fasting for 3 wk or 4-5 mo (natural winter fast) developed an NST of 0.8 and 2.4 W/kg, respectively, despite the fast. In fasting chicks, the intercept of the metabolic curve with the abscissa at zero MR was far below body temperature, contrasting with the classic model for heat loss. Their low LCT indicates the capacity of a large reduction in convective conductance characteristic of diving animals and allows energy sparing in moderate cold. Below LCT, conductance reincreases progressively, leading to a steeper than expected slope of the metabolic curve and allowing preservation of a threshold temperature in the shell. These results show for the first time in a wild young bird the development of NST after cold acclimatization. Further, at the temperature of cold acclimatization, an energy-sparing mechanism is shown in response to long-term fast adaptation.

Mitochondrial phenotypic flexibility enhances energy savings during winter fast in king penguin chicks

“…The significant energy savings found in fasted king penguin chicks at the mitochondrial level was reflected at the whole-animal level with the reduction of resting metabolic rate. The reduction of mass-specific resting metabolic rate observed in fasted chicks is in line with the low level of resting metabolic rate previously reported in chick (Barré, 1984;Duchamp et al, 1989) and adult of king penguins (Fahlman et al, 2004;Rey et al, 2008) after several weeks of fasting. In the present study, the reduction in whole-animal metabolic rate was not ascribed to a difference in body temperature between fasted and re-fed birds.…”

“…Firstly, chicks are anatomically (large size, round shape, high thermal insulation) and behaviourally (huddles) well adapted to minimize heat dissipation in harsh environmental conditions (Barré, 1984;Le Bohec et al, 2005). Secondly, the winter energy expenditure is physiologically reduced by lowering the plasma level of thyroid hormones and the amount of metabolically active tissues, thereby minimizing the basal metabolic rate and the metabolic cost of growth (Barré, 1984;Cherel and Le Maho, 1985;Cherel et al, 1987;Cherel et al, 1993a;Cherel et al, 2004;Duchamp et al, 1989). Thirdly, the development of seasonal heterothermy (Eichhorn et al, 2011), together with a low thermogenic effect of circulating lipids (Teulier et al, 2013), further indicate a reduced energy investment into heat production and thermoregulation.…”

“…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.It remains that skeletal muscle is also the main tissue involved in thermogenesis, an energetically demanding process that remains operative during winter (Barré, 1984;Duchamp et al, 1989). Is there a cost of having more energy efficient mitochondria when these…”

“…The day before experimentation, chicks were fasted. After stabilization within the thermostatic chamber at thermoneutrality, the resting metabolic rate was recorded in vivo by indirect calorimetry as already described in king penguin chicks (Duchamp et al, 1989;Teulier et al, 2013). The day after the indirect calorimetry experiments, ~3 g of the superficial pectoralis muscle was surgically biopsied under isoflurane-induced general anaesthesia and immediately used for mitochondrial extraction (Rey et al, 2008).…”

Differential muscular myosin heavy chain expression of the pectoral and pelvic girdles during early growth in the king penguin (Aptenodytes patagonicus) chick

“…The MyHC adult profile of the PM of young chicks could therefore indicate an early maturation of the contractile muscle proteins that would allow shivering as early as hatching. Furthermore, this muscle is known to be the major source of shivering and non-shivering thermogenesis in adults (Duchamp et al, 1989).…”