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Hypothermia in foraging king penguins

Nature volume 388, pages 64–67 (1997)Cite this article

Abstract

The ability to dive for long periods increases with body size1, but relative to the best human divers, marine birds and mammals of similar or even smaller size are outstanding performers. Most trained human divers can reach a little over 100 m in a single-breath dive lasting for 4 min (ref. 2), but king and emperor penguins (weighing about 12 and 30 kg, respectively) can dive to depths of 304 and 534 m for as long as 7.5 and 15.8 min, respectively3,4,5. On the basis of their assumed metabolic rates, up to half of the dive durations were believed to exceed the aerobic dive limit, which is the time of submergence before all the oxygen stored in the body has been used up4,6,7. But in penguins and many diving mammals7,8, the short surface intervals between dives are not consistent with the recovery times associated with a switch to anaerobic metabolism4. We show here that the abdominal temperature of king penguins may fall to as low as 11 °C during sustained deep diving. As these temperatures may be 10 to 20 °C below stomach temperature, cold ingested food cannot be the only cause of abdominal cooling. Thus, the slower metabolism of cooler tissues resulting from physiological adjustments associated with diving per se, could at least partly explain why penguins and possibly marine mammals can dive for such long durations.

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Figure 1: Sagittal view of the abdominal region of a king penguin showing the location of three recorders: R1, time/temperature recorder located in the stomach; R2, time/temperature/depth recorder implanted in the abdominal fat of the lower abdomen, with an external thermistor placed against the stomach wall; R3, time/temperature/heart rate recorder implanted under the sternum and against the stomach wall in the upper abdomen.
Figure 2: Typical data obtained from a single bird corresponding to: (1) the end of the brooding shift (range, 5–10 d; mean ± s.d.: 7.3 ± 1.9, n = 12); (2) the foraging trip (range 5.1–10.2 d; mean, 7.5 ± 1.6); (3) the beginning of the following brooding shift (less than 36 h).
Figure 3: Representative changes of the three recorded temperatures during different diving activity two days before the end of the foraging trip (bird N departed on 21 February at 08:02 h for 10.5 d of foraging), showing the temporal changes in temperature that occur inside the abdominal cavity.
Figure 4: Short-term variations of the three abdominal temperatures near the end of a deep-diving bout and 1 d before the end of the foraging trip (bird O returns to the chick on 01 March at 16:08 h after 8.2 d at sea).

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References

  1. Kooyman, G. L. Diverse Divers(ed. Farner, D. S.) 1–200 (Springer, Berlin, (1989)).

    Google Scholar 

  2. Corriol, J. H.La Plongée en Apnée. Physiologie et Médecine 2nd edn(Masson, Paris, (1996)).

    Google Scholar 

  3. Kooyman, G. L. et al. Diving behavior and energetics during foraging cycles in king penguins. Ecol. Monogr. 62, 143–163 (1992).

    Article  Google Scholar 

  4. Kooyman, G. L. & Kooyman, T. G. Diving behavior of emperor penguins nurturing chicks at Coulman island, Antarctica. Condor 97, 536–549 (1995).

    Article  Google Scholar 

  5. Ancel, A. et al. Foraging behaviour of emperor penguins as a resource detector in winter and summer. Nature 360, 336–338 (1992).

    Article  ADS  Google Scholar 

  6. Culik, B. M. et al. Diving energetics in king penguins (Aptenodytes patagonicus). J. Exp. Biol. 199, 973–983 (1996).

    CAS  PubMed  Google Scholar 

  7. Kooyman, G. L. et al. Heart rates and swim speeds of emperor penguins diving under sea ice. J. Exp. Biol. 165, 161–180 (1992).

    CAS  PubMed  Google Scholar 

  8. Boyd, I. L. & Croxall, J. P. Dive durations in pinnipeds and seabirds. Can. J. Zool. 74, 1696–1705 (1996).

    Article  Google Scholar 

  9. Guinet, C. et al. Foraging behaviour of satellite-tracked king penguins in relation to the sea surface temperature obtained by satellite telemetry at Crozet Archipelago during the austral summer: a three year study. Mar. Ecol. Prog. Ser.(in the press).

  10. Bost, C. A. et al. Foraging habitat and food intake of satellite-tracked king penguins during the austral summer at Crozet Archipelago. Mar. Ecol. Prog. Ser.(in the press).

  11. Pütz, K. & Bost, C.-A. Feeding behavior of free-ranging king penguins (Aptenodytes patagonicus). Ecology 75, 489–497 (1994).

    Article  Google Scholar 

  12. Wilson, R. P. & Culik, B. M. The cost of a hot meal: facultative specific dynamic action may ensure temperature homeostatis in post-ingestive endotherms. Comp. Biochem. Physiol. 100A, 151–154 (1991).

    Article  Google Scholar 

  13. Wilson, R. P. et al. Reliability of stomach temperature changes in determining feeding characteristics of seabirds. J. Exp. Biol. 198, 1115–1135 (1995).

    CAS  PubMed  Google Scholar 

  14. Pütz, K. Aspects of the feeding ecology of emperor penguins (Aptenodytes forsteri) and king penguins (Aptenodytes patagonicus). Rep. Polar Res. 136, 1–139 (1994).

    Google Scholar 

  15. Hill, D. R. et al. Heart rate and body temperature during free diving of Weddell seals. Am. J. Physiol. 253, R344–R351 (1987).

    CAS  PubMed  Google Scholar 

  16. Ponganis, P. J., Kooyman, G. L., Castellini, M. A., Ponganis, E. P. & Ponganis, K. V. Muscle temperature and swim velocity profiles during diving in a Weddell seal, Leptenychotes weddellii. J. Exp. Biol. 183, 341–348 (1993).

    CAS  PubMed  Google Scholar 

  17. Culik, B. M. et al. Core temperature variability in diving king penguins (Aptenodytes patagonicus): a preliminary analysis. Polar Biol. 16, 371–378 (1996).

    Article  Google Scholar 

  18. Butler, P. J., Bevan, R. M., Woakes, A. J., Croxall, J. P. & Boyd, I. L. The use of data loggers to determine the energetics and physiology of aquatic birds and mammals. Braz. J. Med. Biol. Res. 28, 1307–1317 (1995).

    CAS  PubMed  Google Scholar 

  19. Bevan, R. M. et al. Heart rate and abdominal temperatures of free-ranging South Georgian shags, Phalacrocorax georgianus. J. Exp. Biol. 200, 661–675 (1997).

    CAS  PubMed  Google Scholar 

  20. Wilson, R. P., Cooper, J. & Plötz, J. Can we determine when marine endotherms feed? J. Exp. Biol. 167, 267–275 (1992).

    Google Scholar 

  21. Woakes, A. J., Butler, P. J., Bevan, R. M. & Boyd, I. L. The metabolic rate of free ranging antarctic animals. Biotelemetry XII 21, 3–223 (1992).

    Google Scholar 

  22. Woakes, A. J., Butler, P. J. & Bevan, R. M. Implantable data logging system for heart rate and body temperature: its application ot the estimation of field metabolic rates in Antarctic predators. Med. Biol. Eng. Comput. 33, 145–151 (1995).

    Article  CAS  Google Scholar 

  23. Scholander, P. F., Irving, L. & Grinnel, S. W. On the temperature and metabolism of the seal during diving. J. Cell Comp. Physiol. 19, 67–78 (1942).

    Article  CAS  Google Scholar 

  24. Bevan, R. M. & Butler, P. J. Cardiac output and blood flow distribution during swimming and voluntary diving of the tufted duck (Aythya fuligula). J. Exp. Biol. 168, 199–217 (1992).

    Google Scholar 

  25. Carey, F. G. A Companion to Animal Physiology(eds Taylor, C. R., Johnsen, K. & Bolis, L.) 216–235 (Cambridge Univ. Press, (1982)).

    Google Scholar 

  26. Kooyman, G. L., Wahrenbrock, E. A., Castellini, M. A., Davis, R. W. & Sinnett, E. E. Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior. J. Comp. Physiol. 138, 335–346 (1980).

    Article  CAS  Google Scholar 

  27. Ketterson, E. D. & King, J. R. Metabolic and behavioral responses to fasting in the white-crowned sparrow (Zonotrichia leucophrys gambelli). Physiol. Zool. 50, 115–129 (1977).

    Article  Google Scholar 

  28. Heldmaier, G., Steiger, R. & Ruf, T. Life in the Cold. Ecological, Physiological and Molecular Mechanisms(eds Carey, C., Florant, G. L., Wunder, B. A. & Horwitz, B.) 545–548 (Westview, Boulder, (1993)).

    Google Scholar 

  29. Ruf, T. & Heldmaier, G. The impact of daily torpor on energy requirements in the Djungarian hamster, Phodopus sungorus. Physiol. Zool. 65, 994–1010 (1992).

    Article  Google Scholar 

  30. Heller, H. C., Elsner, R. & Rao, N. Voluntary hypometabolism in an Indian yogi. J. Therm. Biol. 12, 171–173 (1987).

    Article  Google Scholar 

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Acknowledgements

We thank G. Froget, Y. Ropert-Coudert, J.-N. Clech and all the 1995 winter team in Crozet for their assistance in the field, and A. Ancel, C.-A. Bost, B. M. Culik and A. Malan for comments on the manuscript. After approval by the ethics committee of the Institut Français pour la Recherche et la Technologie Polaires, this study was supported by a grant for this Institute and by an NERC Small Research grant.

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Authors and Affiliations

  1. *Centre d'Ecologie et Physiologie Energtiques, Centre National de la Recherche Scientifique, 23 rue Becquerel, 67087, Strasbourg, cedex 2, France

    Y. Handrich, J.-B. Charrassin, J. Lage & Y. Le Maho

  2. †School of Biological Sciences, University of Birmingham, Edgbaston, B15 2TT, Birmingham, UK

    R. M. Bevan, P. J. Butler & A. J. Woakes

  3. ‡Abteilung Meereszoologie, Institut für Meereskunde, Düsternbrooker Weg 20, Kiel, D-24105, Germany

    K. Ptz

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Correspondence to Y. Handrich.

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Handrich, Y., Bevan, R., Charrassin, JB. et al. Hypothermia in foraging king penguins. Nature 388, 64–67 (1997). https://doi.org/10.1038/40392

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