Energy conservation is a key priority for organisms that live in environments with seasonal shortages in resource supplies or that spontaneously fast during their annual cycle. The aim of this study was to determine whether the high fasting endurance of winteracclimatized king penguin chicks (Aptenodytes patagonicus) is associated with an adjustment of mitochondrial bioenergetics in pectoralis muscle, the largest skeletal muscle in penguins. The rates of mitochondrial oxygen consumption, and ATP synthesis and mitochondrial efficiency (ATP/O ratio) were measured in winteracclimatized chicks. We used pyruvate/malate and palmitoyl-Lcarnitine/malate as respiratory substrates and results from naturally fasted chicks were compared to experimentally re-fed chicks. Bioenergetics analysis of pectoralis muscle revealed that mitochondria are on average 15% more energy efficient in naturally fasted than in experimentally fed chicks, indicating that fasted birds consume less nutrients to sustain their energy-demanding processes. We also found that moderate reductions in temperature from 38°C to 30°C further increase by 23% the energy coupling efficiency at the level of mitochondria, suggesting that king penguin chicks realize additional energy savings while becoming hypothermic during winter. It has been calculated that this adjustment of mitochondrial efficiency in skeletal muscle may contribute to nearly 25% of fasting-induced reduction in mass-specific metabolic rate measured in vivo. The present study shows that the regulation of mitochondrial efficiency triggers the development of an economical management of resources, which would maximize the conservation of endogenous fuel stores by decreasing the cost of living in fasted winteracclimatized king penguin chicks. KEY WORDS: Bird, Skeletal muscle, Mitochondria, Energy efficiency, Starvation INTRODUCTIONSpontaneous fast is a major characteristic of the annual cycle of sea birds when breeding or moulting on land, whereas they feed exclusively at sea. In situations where food is lacking or not used, the allocation of limited endogenous resources causes trade-offs between competing traits, such as reproduction, somatic growth and maintenance. During food deprivation, animals cannot maximize all of their life-history traits and must exhibit adaptive behavioural, physiological and biochemical responses to reduce metabolism and/or the cost of current activities in order to maintain biological value (Wang et al., 2006). Among sea birds, penguins, especially the Aptenodytes genus, which inhabits cold environments, have evolved to tolerate some of the greatest relative body mass losses and to survive several months of starvation, which can be up to 5 months in winter-acclimatized king penguin chicks (Cherel and Le Maho, 1985;Groscolas, 1990;McCue, 2010). RESEARCH ARTICLEKing penguin chicks (Aptenodytes patagonicus, Miller J. F. 1778) experience a severe nutritional shortage when left alone for a long period of time, and they may be fed infrequently or not at all by their p...
At fledging, juvenile king penguins (Aptenodytes patagonicus) must overcome the tremendous energetic constraints imposed by their marine habitat, including during sustained extensive swimming activity and deep dives in cold seawater. Both endurance swimming and skeletal muscle thermogenesis require high mitochondrial respiratory capacity while the submerged part of dive cycles repeatedly and greatly reduce oxygen availability imposing a need for solutions to conserve oxygen. The aim of the present study was to determine in vitro whether skeletal muscle mitochondria become more “thermogenic” to sustain heat production or more “economical” to conserve oxygen in sea-acclimatized immature penguins as compared with terrestrial juveniles. Rates of mitochondrial oxidative phosphorylation were measured in permeabilized fibers and mitochondria from the pectoralis muscle. Mitochondrial ATP synthesis and coupling efficiency were measured in isolated muscle mitochondria. The mitochondrial activities of respiratory chain complexes and citrate synthase were also assessed. The results showed that respiration, ATP synthesis and respiratory chain complex activities in pectoralis muscles were increased by sea acclimatization. Further, muscle mitochondria were on average 30% to 45% more energy efficient in sea-acclimatized immatures than in pre-fledging juveniles, depending on the respiratory substrate used (pyruvate; palmitoyl-carnitine). Hence, sea acclimatization favors the development of economical management of oxygen, decreasing the oxygen needed to produce a given amount of ATP. This mitochondrial phenotype may improve dive performance during the early marine life of king penguins, by extending their aerobic dive limit.
Environmental constraints are strong in migratory species that breed in the Arctic. In addition to breeding, Anatidae have to renew all their fl ight feathers during the short arctic summer. We examine how temporal constraints and climate aff ect the phenology of fl ight feather moult in the greater snow goose Chen caerulescens atlantica , a High Arctic nesting species. We used a database of 1412 moulting adult females measured over 15 yr on Bylot Island, Nunavut. Ninth (9th) primary length was used to determine the moult stage and speed of feather growth. We found a positive relationship between median annual hatching and moult initiation dates and the slope did not diff er from 1. Th e interval between hatching and moult initiation was thus rather fi xed and geese did not initiate moult earlier when reproductive phenology was delayed. Nonetheless, there was no relationship between median hatching date and the date at which birds regained fl ight capacity, suggesting that date of end of moult is independent of the reproductive phenology. Th ere was a trend for an increase in the speed of fl ight feather growth in years with delayed hatching date. Th is is the most likely mechanism that could explain moult phenology adjustment in this species. Finally, we found a positive relationship between 9th primary length (corrected for inter-annual variations) and body condition, suggesting a delay in moulting for individuals in poor condition. Th ese results suggest that moult plasticity is primarily governed by variations in feather growth speed. Th is phenotypic plasticity could be necessary to complete fl ight feather renewal before the end of the arctic summer, independently of reproductive phenology and spring environmental conditions. Our novel results suggest possible phenological adjustments through moult speed, which was considered constant in geese until now.
The Arctic is undergoing numerous environmental transformations. As a result of rising temperatures and additional freshwater inputs, ice cover is changing, with profound impacts on organisms at the base of food webs and consequently on the entire Arctic ecosystem. Indeed, phytoplankton not only provide energy as lipids, but also essential fatty acids (EFA) that animals cannot synthesize and must acquire in their diet. Omega-3 (ω3) and omega-6 (ω6) polyunsaturated fatty acids (PUFA) are essential for the healthy development and function of organisms. The high energy potential of monounsaturated fatty acids (MUFA) is of particular importance in cold waters, and various fatty acids including saturated fatty acids (SFA) are involved in organismal responses to environmental stressors. Yet relatively little is known of how variability or change in physicochemical seawater properties (e.g., temperature, light, salinity, pH and nutrients) may affect lipid synthesis in polar environments, either directly, by altering algal physiology, or indirectly, by promoting shifts in phytoplankton species composition. Here we investigated these two possibilities by sampling along a 3,000-km transect spanning 28 degrees of latitude across the subarctic and Arctic domains of Canada. The taxonomic composition of phytoplankton mainly drove the FA profiles measured in particulate organic matter (POM). Strong, positive correlations between 16:1ω7 and diatoms were observed while the proportion of PUFA and ω6 FA increased with flagellate abundance. Among specific FAs, eicosapentaenoic acid (EPA; 20:5ω3) was positively correlated with diatoms but the expected relationship between docosahexaenoic acid (DHA; 22:6ω3) and dinoflagellates was not observed. Decreasing pH had a negative effect on EPA and MUFA proportions, and DHA proportions tended to decrease with higher temperature. These two effects were primarily driven by differences in phytoplankton assemblage composition. Overall, the results of this geographically extensive study provide new information into the use of lipid markers and the ecological determinants of FA synthesis in the North. It also highlights the importance of long-lived subsurface chlorophyll maximum layers in supplying PUFA-rich POM to the food web and suggests that this situation may persist despite ongoing changes in the physical environment.
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