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

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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.

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Acknowledgments

The project was supported financially and logistically by the French Polar Institute (Institut Paul Emile Victor, IPEV—research program no. 131), and received a logistic support from the Terres Australes et Antarctiques Françaises.

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Authors and Affiliations

  1. Laboratoire d’Ecologie des Hydrosystèmes Naturels et Anthropisés, UMR 5023 CNRS, Université Claude Bernard Lyon 1, ENTPE, Lyon, Bâtiment Charles Darwin C, 69622, Villeurbanne cedex, France

    Loïc Teulier, Jérémy Tornos, Marion Le Coadic, Pierre-Axel Monternier, Aurore Bourguignon, Virginie Dolmazon, Caroline Romestaing, Jean-Louis Rouanet, Claude Duchamp & Damien Roussel

  2. Laboratoire de Biométrie et Biologie Evolutive, UMR 5558 CNRS, Université Claude Bernard Lyon 1, 69622, Villeurbanne cedex, France

    Benjamin Rey

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  1. Loïc Teulier
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  2. Benjamin Rey
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  4. Marion Le Coadic
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  9. Jean-Louis Rouanet
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Correspondence to Damien Roussel.

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Communicated by G. Heldmaier.

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Teulier, L., Rey, B., Tornos, J. et al. Lipid-induced thermogenesis is up-regulated by the first cold-water immersions in juvenile penguins. J Comp Physiol B 186, 639–650 (2016). https://doi.org/10.1007/s00360-016-0975-3

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  • DOI: https://doi.org/10.1007/s00360-016-0975-3

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