Heterothermy in growing king penguins

Eichhorn, Götz; Groscolas, René; Glaunec, Gaële Le; Parisel, Camille; Arnold, Laurent; Medina, Patrice; Handrich, Yves

doi:10.1038/ncomms1436

Cited by 38 publications

(35 citation statements)

References 33 publications

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“…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.…”

Section: The Journal Of Experimental Biologymentioning

confidence: 99%

“…Hence, changes in skeletal muscle mitochondrial efficiency would have no major impact on the intrinsic capacity of a chick's thermogenic mechanism during phase II of fasting. In conclusion, the regulation of the degree of mitochondrial coupling reported in fasted winter-acclimatized chicks triggers an economical management of resources at the level of mitochondria, which would, in association with short-term hypothermic stage, maximize the conservation of endogenous fuel stores and may contribute to the ability of king penguins to withstand fasting for several months (Cherel and Le Maho, 1985;Cherel et al, 1993a;Eichhorn et al, 2011). …”

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

Monternier

Marmillot

Rouanet

et al. 2014

Journal of Experimental Biology

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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...

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Section: The Journal Of Experimental Biologymentioning

confidence: 99%

mentioning

confidence: 99%

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

Monternier

Marmillot

Rouanet

et al. 2014

Journal of Experimental Biology

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“…Such a decline in heart rate should indicate the presence of a developed dive reflex (including a vasomotor response; Butler and Jones, 1997). The strong decline in peripheral temperature observed in king penguin chicks during their winter fast also indicates the presence of an effective vasomotor control, months before they go to sea (Eichhorn et al, 2011).…”

Section: Potential Physiological Maturation Of the Thermoregulatory Rmentioning

confidence: 99%

“…During whole-body immersions in the laboratory, juvenile king and gentoo penguins (Pygoscelis papua) showed a gradual increase in internal insulation over time, suggesting that the peripheral vasoconstriction response was not fully developed upon first immersion (Barré and Roussel, 1986;Dumonteil et al, 1994). By contrast, Eichhorn et al (2011) reported a remarkable heterothermy in the body core and in peripheral tissues of free-living king penguin chicks throughout the winter period, when they fast for up to 5 months, in air (Cherel and Le Maho, 1985). Subcutaneous temperatures as low as 19°C and a temperature gradient between the core and the shell of up to 15.7°C were measured, indicating the presence of a peripheral vasoconstrictive response, long before their first departure to sea (Eichhorn et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…By contrast, Eichhorn et al (2011) reported a remarkable heterothermy in the body core and in peripheral tissues of free-living king penguin chicks throughout the winter period, when they fast for up to 5 months, in air (Cherel and Le Maho, 1985). Subcutaneous temperatures as low as 19°C and a temperature gradient between the core and the shell of up to 15.7°C were measured, indicating the presence of a peripheral vasoconstrictive response, long before their first departure to sea (Eichhorn et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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

Enstipp

Bost

Bohec

et al. 2017

Journal of Experimental Biology

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Little is known about the early life at sea of marine top predators, like deep-diving king penguins (Aptenodytes patagonicus), although this dispersal phase is probably a critical phase in their life. Apart from finding favourable foraging sites, they have to develop effective prey search patterns as well as physiological capacities that enable them to capture sufficient prey to meet their energetic needs. To investigate the ontogeny of their thermoregulatory responses at sea, we implanted 30 juvenile king penguins and 8 adult breeders with a small data logger that recorded pressure and subcutaneous temperature continuously for up to 2.5 years. We found important changes in the development of peripheral temperature patterns of foraging juvenile king penguins throughout their first year at sea. Peripheral temperature during foraging bouts fell to increasingly lower levels during the first 6 months at sea, after which it stabilized. Most importantly, these changes re-occurred during their second year at sea, after birds had fasted for ∼4 weeks on land during their second moult. Furthermore, similar peripheral temperature patterns were also present in adult birds during foraging trips throughout their breeding cycle. We suggest that rather than being a simple consequence of concurrent changes in dive effort or an indication of a physiological maturation process, these seasonal temperature changes mainly reflect differences in thermal insulation. Heat loss estimates for juveniles at sea were initially high but declined to approximately half after ∼6 months at sea, suggesting that juvenile king penguins face a strong energetic challenge during their early oceanic existence.

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Optimal sampling interval for characterisation of the circadian rhythm of body temperature in homeothermic animals using periodogram and cosinor analysis

Goh,

Vesterdorf,

Fuller

et al. 2024

Ecology and Evolution

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Core body temperature (Tc) is a critical aspect of homeostasis in birds and mammals and is increasingly used as a biomarker of the fitness of an animal to its environment. Periodogram and cosinor analysis can be used to estimate the characteristics of the circadian rhythm of Tc from data obtained on loggers that have limited memory capacity and battery life. The sampling interval can be manipulated to maximise the recording period, but the impact of sampling interval on the output of periodogram or cosinor analysis is unknown. Some basic guidelines are available from signal analysis theory, but those guidelines have never been tested on Tc data. We obtained data at 1‐, 5‐ or 10‐min intervals from nine avian or mammalian species, and re‐sampled those data to simulate logging at up to 240‐min intervals. The period of the rhythm was first analysed using the Lomb–Scargle periodogram, and the mesor, amplitude, acrophase and adjusted coefficient of determination (R2) from the original and the re‐sampled data were obtained using cosinor analysis. Sampling intervals longer than 60 min did not affect the average mesor, amplitude, acrophase or adjusted R2, but did impact the estimation of the period of the rhythm. In most species, the period was not detectable when intervals longer than 120 min were used. In all individual profiles, a 30‐min sampling interval modified the values of the mesor and amplitude by less than 0.1°C, and the adjusted R2 by less than 0.1. At a 30‐min interval, the acrophase was accurate to within 15 min for all species except mice. The adjusted R2 increased as sampling frequency decreased. In most cases, a 30‐min sampling interval provides a reliable estimate of the circadian Tc rhythm using periodogram and cosinor analysis. Our findings will help biologists to select sampling intervals to fit their research goals.

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Heterothermy in growing king penguins

Cited by 38 publications

References 33 publications

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

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

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

Optimal sampling interval for characterisation of the circadian rhythm of body temperature in homeothermic animals using periodogram and cosinor analysis

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