Skip to main content
SpringerLink
Log in

Protein and lipid utilization during fasting with shallow and deep hypothermia in the European hedgehog (Erinaceus europaeus)

  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

We investigated whether the relative contributions of body protein and lipid reserves differ according to the level of energy expenditure in fasting animals. Protein and lipid utilization was therefore quantified and compared in hedgehogs which fasted with shallow and deep hypothermia, i.e. by exposure at 5 or 20 °C ambient temperature. Body composition was determined for every 150-g decrease in mass throughout the experiment, allowing the calculation of regression lines between body mass (independent variable, x) and body composition (dependent variable, y: water, protein, neutral lipids, phospholipids and cholesterol). There were highly significant (P<0.001) linear decreases in all body components with decreasing body mass in both groups of hedgehogs. Neutral lipids were the main component of the total body mass loss (54%) in fasted animals with shallow and deep hypothermia, percentages of water (26–30%) and protein (10–11%) being lower, and those of phospholipid and cholesterol negligible (<0.5%). In spite of different levels in energy expenditure (2.54 and 1.07 W·kg-1 in shallow-and deep-hypothermal fasting hedgehogs, respectively), the energy sources were identical in both groups, neutral lipid being the main fuel (91–92%) and body protein accounting for the remainder (8–9%). Prolonged fasting with shallow and deep hypothermia were marked by low alaninemia and glycemia, while plasma free fatty acids and β-hydroxybutyrate were elevated. These data therefore indicate that the relative contribution of lipid and protein is similar during prolonged fasting with shallow and deep hypothermia, i.e. there is no specific effect of deep hypothermia on body fuel utilization. The tolerance of a much longer fast in deep-hypothermal hedgehogs can simply be attributed to the lower rates of lipid and protein utilization as a result of the lower level of energy expenditure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

bm:

body mass

References

  • Barré H (1984) Metabolic and insulative changes in winter- and summer-acclimatized king penguin chicks. J Comp Physiol B 154:317–324

    Google Scholar 

  • Bartlett GR (1959) Phosphorus assay in column chromatography. J Biol Chem 234:466–468

    Google Scholar 

  • Bartness TJ, Milner R, Geloen A, Trayhurn P (1991) Effects of high fat diets on hibernation and adipose tissue in Turkish hamsters. J Comp Physiol B 161:451–459

    Google Scholar 

  • Cahill GF, Marliss EB, Aoki TT (1970) Fat and nitrogen metabolism in fasting man. In: Jeanrenaud B, Hepp D (eds) Adipose tissue: regulation and metabolic functions. Academic Press, New York, pp 181–185

    Google Scholar 

  • Castellini MA, Rea LD (1992) The biochemistry of natural fasting at its limits. Experientia 48:575–582

    Google Scholar 

  • Cherel Y, Le Maho Y (1985) Five months of fasting in king penguin chicks: body mass loss and fuel metabolism. Am J Physiol 249 (Regul Integr Comp Physiol 18):R387–R392

    Google Scholar 

  • Cherel Y, Ridoux V (1992) Prey species and nutritive value of food fed during summer to king penguin Aptenodytes patagonica chicks at Possession Island, Crozet Archipelago. Ibis 134:118–127

    Google Scholar 

  • Cherel Y, Robin JP, Le Maho Y (1988) Physiology and biochemistry of long-term fasting in birds. Can J Zool 66:159–166

    Google Scholar 

  • Cherel Y, Robin JP, Heitz A, Calgari C, Le Maho Y (1992) Relationships between lipid availability and protein utilization during prolonged fasting. J Comp Physiol B 162:305–313

    Google Scholar 

  • Cherel Y, Fréby F, Gilles J, Robin JP (1993) Comparative fuel metabolism in gentoo and king penguins: adaptation to brief versus prolonged fasting. Polar Biol 13:263–269

    Google Scholar 

  • Cherel Y, Gilles J, Handrich Y, Le Maho Y (1994) Nutrient reserve dynamics and energetics during long-term fasting in the king penguin (Aptenodytes patagonicus). J Zool (London) 234:1–12

    Google Scholar 

  • Cranford JA (1978) Hibernation in the western jumping mouse (Zapus princeps). J Mamm 59:496–509

    Google Scholar 

  • Florant GL, Nuttle LC, Mullinex DE, Rintoul DA (1990) Plasma and white adipose tissue lipid composition in marmots. Am J Physiol 258 (Regul Integr Comp Physiol 27):R1123–R1131

    Google Scholar 

  • Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    Google Scholar 

  • Folk GE (1957) Twenty-four hour rhythms of mammals in a cold environment. Am Nat 91:153–166

    Google Scholar 

  • Fowler PA, Racey PA (1990) Daily and seasonal cycles of body temperature and aspects of heterothermy in the hedgehog Erinaceus europaeus. J Comp Physiol B 160:299–307

    Google Scholar 

  • Galster W, Morrison P (1976) Seasonal changes in body composition of the arctic ground squirrel, Citellus undulatus. Can J Zool 54:74–78

    Google Scholar 

  • Goodman MN, Larsen PR, Kaplan MM, Aoki TT, Young VR, Ruderman NB (1980) Starvation in the rat. II. Effect of age and obesity on protein sparing and fuel metabolism. Am J Physiol 239 (Endocrinol Metab 2):E277–E286

    Google Scholar 

  • Groscolas R (1990) Metabolic adaptations to fasting in emperor and king penguins. In: Davis LS, Darby JT (eds) Penguin biology. Academic Press, San Diego, pp 269–296

    Google Scholar 

  • Groscolas R, Schreiber L, Morin F (1991) The use of tritiated water to determine protein and lipid utilization in fasting birds: a validation technique in incubating great-winged petrels, Pterodroma macroptera. Physiol Zool 64:1217–1233

    Google Scholar 

  • Harper JF (1984) Peritz' F-test: basic program of a robust multiple comparison test for statistical analysis of all differences among group means. Comput Biol Med 14:437–445

    Google Scholar 

  • Kates M (1972) Techniques of lipidology. North Holland, Amsterdam, pp 360–361

    Google Scholar 

  • Kayser C (1961) The physiology of natural hibernation. Academic Press, Oxford

    Google Scholar 

  • Krilowicz BL (1985) Ketone body metabolism in a ground squirrel during hibernation and fasting. Am J Physiol 249 (Regul Integr Comp Physiol 18):R462-R470

    Google Scholar 

  • Kristoffersson R, Suomalainen P (1964) Studies on the physiology of the hibernating hedgehog. 2. Changes of body weight of hibernating and non-hibernating animals. Ann Acad Sci Fenn Ser A 76:1–11

    Google Scholar 

  • Le Maho Y, Robin JP, Cherel Y (1988) Starvation as a treatment for obesity: the need to conserve body protein. News Physiol Sci 3:21–24

    Google Scholar 

  • Maxwell RK, Thorkelson J, Rogers LL, Brander RB (1988) The field energetics of winter-dormant black bear (Ursus americanus) in northeastern Minnesota. Can J Zool 66:2095–2103

    Google Scholar 

  • Morris P (1984) An estimate of the minimum body weight necessary for hedgehogs (Erinaceus europaeus) to survive hibernation. J Zool (London) 203:291–294

    Google Scholar 

  • Nelson RA (1980) Protein and fat metabolism in hibernating bears. Fed Proc 39:2955–2958

    Google Scholar 

  • Piersma T, Jukema J (1990) Budgeting the flight of a long-distance migrant: changes in nutrient reserve levels of bar-tailed godwits at successive spring staging sites. Ardea 78:315–337

    Google Scholar 

  • Rauch JC, Behrisch HW (1981) Ketone bodies: a source of energy during hibernation. Can J Zool 59:754–760

    Google Scholar 

  • Riedesel ML, Steffen JM (1980) Protein metabolism and urea recycling in rodent hibernators. Fed Proc 39:2959–2963

    Google Scholar 

  • Robin JP, Cherel Y, Girard J, Géloen A, Le Maho Y (1987) Uric acid and urea in relation to protein catabolism in long-term fasting geese. J Comp Physiol B 157:491–499

    Google Scholar 

  • Saboureau M (1986) Hibernation in the hedgehog: influence of external and internal factors. In: Heller HC et al. (eds) Living in the cold. Physiological and biochemical adaptations. Elsevier, New York, pp 253–263

    Google Scholar 

  • Saboureau M, Castaing L, Boissin J (1984) Influence du taux plasmatique de testostérone et du jeûne sur les variations automnales et hivernales de l'activité motrice générale du Hérisson, Erinaceus europaeus L. CR Acad Sci Sér III 299:239–244

    Google Scholar 

  • Saboureau M, Cherel Y, El Omari B, Le Maho Y (1991a) Contribution des protéines et des lipides à la dépense énergétique du Hérisson à jeun avec ou sans hibernation. Arch Int Physiol Biochim Biophys 99:A175

    Google Scholar 

  • Saboureau M, Vignault MP, Ducamp JJ (1991b) L'hibernation chez le Hérisson (Erinaceus europaeus L.) dans son environnement naturel: étude par biotélémétrie des variations de la température corporelle. CR Acad Sci Paris Sér III 313:93–100

    Google Scholar 

  • Schmidt-Nielsen K (1979) Animal physiology: adaptation and environment, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Tähti H (1978) Seasonal differences in O2 consumption and respiratory quotient in a hibernator (Erinaceus europaeus L.). Ann Zool Fenn 15:69–75

    Google Scholar 

  • Willis JS (1982) Intermediary metabolism in hibernation. In: Lyman CP et al. (eds) Hibernation and torpor in mammals and birds. Academic Press, New York

    Google Scholar 

  • Yacoe ME (1983) Protein metabolism in the pectoralis muscle and liver of hibernating bats, Eptesicus fuscus. J Comp Physiol B 152:137–144

    Google Scholar 

Download references

Author information

Author notes

  1. Y. Cherel

    Present address: CEBC CNRS, Villiers en Bois, F-79360, Beauvoir sur Niort, France

  2. M. Saboureau

    Present address: Laboratoire de Neurobiologie des Fonctions Rythmiques et Saisonnières, URA 1332-CNRS, Université Louis Pasteur, 12 rue de l'Université, F-67000, Strasbourg, France

Authors and Affiliations

  1. Centre d'Ecologie et Physiologie Energétiques, Centre National de la Recherche Scientifique, 23 rue Becquerel, F-67087, Strasbourg, France

    Y. Cherel & Y. Le Maho

  2. Centre d'Etudes Biologiques de Chizé, Centre National de la Recherche Scientifique, Villiers en Bois, F-79360, Beauvoir sur Niort, France

    B. El Omari & M. Saboureau

Authors
  1. Y. Cherel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. El Omari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Le Maho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Saboureau
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cherel, Y., El Omari, B., Le Maho, Y. et al. Protein and lipid utilization during fasting with shallow and deep hypothermia in the European hedgehog (Erinaceus europaeus). J Comp Physiol B 164, 653–658 (1995). https://doi.org/10.1007/BF00389807

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00389807

Key words

Search

Navigation