Journal of Comparative Physiology B

, Volume 174, Issue 1, pp 1–12 | Cite as

Physiological adaptations of the raccoon dog (Nyctereutes procyonoides) to seasonal fasting-fat and nitrogen metabolism and influence of continuous melatonin treatment

  • A.-M. Mustonen
  • P. Nieminen
  • M. Puukka
  • J. Asikainen
  • S. Saarela
  • S.-L. Karonen
  • J. V. K. Kukkonen
  • H. Hyvärinen
Original Paper


The raccoon dog (Nyctereutes procyonoides) is a middle-sized canid with profound autumnal fattening followed by winter sleep. This study investigated the effects of prolonged fasting-induced winter sleep on the fat and nitrogen metabolism of the species. Half of the animals were treated with continuous-release melatonin implants to induce artificial short photoperiod. Autumnal accumulation of fat was characterized by low plasma free fatty acid (FFA), diacylglycerol (DG), and triacylglycerol (TG) levels. After transition to winter catabolism, the circulating lipid levels increased due to enhanced lipolysis. Two months of fasting resulted in a steady 3.1 kg weight loss (28% of body mass, 0.47% day−1). Storage fat was mobilized during the winter sleep reflected by the elevated FFA and DG concentrations. The lowered insulin levels could be a stimulator for TG hydrolysis. The plasma total amino acid concentrations, urea levels, and urea-creatinine ratios decreased due to fasting, whereas ammonia and total protein concentrations remained stable. The effects of melatonin on energy metabolism were modest. The results indicate that the raccoon dog is well adapted to long-term wintertime fasting utilizing fat as the principal metabolic fuel. The species can maintain its protein catabolism constant for at least 60 days. Decreased cortisol and thyroid hormone concentrations may contribute to protein sparing.

Key words

Fasting Lipids Nitrogen metabolism Nyctereutes procyonoides Raccoon dog 



amino acids






analysis of variance




body mass


body mass index








free fatty acids


growth hormone








metabolic rate






















ambient temperature


total amino acids


body temperature




total lipids


total protein




white adipose tissue



We thank Mrs. Anita Kervinen for laboratory analyses and Mr. Kasper Heikkilä for technical assistance. Financial support was provided by the Helve Foundation and the Faculty of Science of the University of Joensuu. This experiment complies with the current laws of Finland.

Supplementary material

Supplement 1 + 2

supplements1-2.pdf (30 kb)
(PDF 30 KB)


  1. Abumrad NN, Yazigi N, Cersosimo E, Hourani H, Gedde S, Bulus N, Williams P (1990) Glutamine metabolism during starvation. J Parenter Enteral Nutr 14:71S-76SGoogle Scholar
  2. Asikainen J, Mustonen A-M, Nieminen P, Pasanen S, Araja-Matilainen H, Hyvärinen H (2002) Reproduction of the raccoon dog (Nyctereutes procyonoides) after feeding or food deprivation in winter. J Anim Physiol Anim Nutr (Berl) 86:367–375Google Scholar
  3. Azizi F, Mannix JE, Howard D, Nelson RA (1979) Effect of winter sleep on pituitary-thyroid axis in American black bear. Am J Physiol 237:E227–E230PubMedGoogle Scholar
  4. Bauman WA, Meryn S, Florant GL (1987) Pancreatic hormones in the nonhibernating and hibernating golden mantled ground squirrel. Comp Biochem Physiol A 86:241–244CrossRefPubMedGoogle Scholar
  5. Bruijne JJ de, Koster P de (1983) Glycogenolysis in the fasting dog. Comp Biochem Physiol B 75:553–555CrossRefPubMedGoogle Scholar
  6. Cahill GF Jr (1976) Starvation in man. Clin Endocrinol Metab 5:397–415Google Scholar
  7. Cherel Y, Robin J-P, Le Maho Y (1988) Physiology and biochemistry of long-term fasting in birds. Can J Zool 66:159–166Google Scholar
  8. Cherel Y, El Omari B, Le Maho Y, Saboureau M (1995) Protein and lipid utilization during fasting with shallow and deep hypothermia in the European hedgehog (Erinaceus europaeus). J Comp Physiol B 164:653–658PubMedGoogle Scholar
  9. Council of the European Union (1993) Council Directive 93/119/EC of 22 December 1993 on the protection of animals at the time of slaughter or killingGoogle Scholar
  10. Curthoys NP, Watford M (1995) Regulation of glutaminase activity and glutamine metabolism. Annu Rev Nutr 15:133–159CrossRefPubMedGoogle Scholar
  11. DelGiudice GD, Seal US, Mech LD (1987) Effects of feeding and fasting on wolf blood and urine characteristics. J Wildl Manage 51:1–10Google Scholar
  12. Espat NJ, Copeland EM, Souba WW (1993) Influence of fasting on glutamine transport in rat liver. J Parenter Enter Nutr 17:493–500Google Scholar
  13. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509Google Scholar
  14. Franzmann AW, Schwartz CC (1988) Evaluating condition of Alaskan black bears with blood profiles. J Wildl Manage 52:63–70Google Scholar
  15. Fuglei E (2000) Physiological adaptations of the arctic fox to high Arctic conditions. PhD Dissertation, University of Oslo, NorwayGoogle Scholar
  16. Goldberg AL, Chang TW (1978) Regulation and significance of amino acid metabolism in skeletal muscle. Fed Proc 37:2301–2307PubMedGoogle Scholar
  17. Goldberg AL, Tischler M, DeMartino G, Griffin G (1980) Hormonal regulation of protein degradation and synthesis in skeletal muscle. Fed Proc 39:31–36PubMedGoogle Scholar
  18. 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:E277–E286PubMedGoogle Scholar
  19. Harlow HJ (1981) Torpor and other physiological adaptations of the badger (Taxidea taxus) to cold environments. Physiol Zool 54:267–275Google Scholar
  20. Harlow HJ, Seal US (1981) Changes in hematology and metabolites in the serum and urine of the badger, Taxidea taxus, during food deprivation. Can J Zool 59:2123–2128Google Scholar
  21. Harlow HJ, Nelson RA (1990) Seasonal serum urea-creatinine ratios in wild and captive American badgers, Taxidea taxus. Comp Biochem Physiol A 95:65–68CrossRefPubMedGoogle Scholar
  22. Harlow HJ, Beck TDI, Walters LM, Greenhouse SS (1990) Seasonal serum glucose, progesterone, and cortisol levels of black bears (Ursus americanus). Can J Zool 68:183–187Google Scholar
  23. Hellgren EC, Vaughan MR, Kirkpatrick RL, Scanlon PF (1990) Serial changes in metabolic correlates of hibernation in female black bears. J Mammal 71:291–300Google Scholar
  24. Hellgren EC, Rogers LL, Seal US (1993) Serum chemistry and hematology of black bears: physiological indices of habitat quality or seasonal patterns? J Mammal 74:304–315Google Scholar
  25. Heptner VG, Naumov NP, Jürgenson PB, Sludski AA, Cirkova AF, Bannikov AG (1974) Gattung Nyctereutes Temminck 1839, Marderhunde oder Mangute. In: Heptner VG, Naumov NP (eds) Der Säugetiere der Sowjetunion, Band II: Seekühe und Raubtiere. VEB Gustav Fischer, German Democratic Republic, pp 67–97Google Scholar
  26. Herminghuysen D, Vaughan M, Pace RM, Bagby G, Cook CB (1995) Measurement and seasonal variations of black bear adipose lipoprotein lipase activity. Physiol Behav 57:271–275CrossRefPubMedGoogle Scholar
  27. Hissa R, Siekkinen J, Hohtola E, Saarela S, Hakala A, Pudas J (1994) Seasonal patterns in the physiology of the European brown bear (Ursus arctos arctos) in Finland. Comp Biochem Physiol A 109:781–791PubMedGoogle Scholar
  28. Hugues J-N, Burger AG, Grouselle D, Voirol M-J, Chabert P, Modigliani E, Sebaoun J (1983) Evidence of a thyrotropin-releasing hormone-dependent increase in plasma thyrotropin during refeeding of starved rats. Endocrinology 112:715–719PubMedGoogle Scholar
  29. Kaloyianni M, Freedland RA (1990) Effect of diabetes and time after in vivo insulin administration on ketogenesis and gluconeogenesis in isolated rat hepatocytes. Int J Biochem 22:159–164CrossRefPubMedGoogle Scholar
  30. Kauhala K (1992) Ecological characteristics of the raccoon dog in Finland. PhD Dissertation, University of Helsinki, FinlandGoogle Scholar
  31. Korhonen H (1987) Energy metabolism of raccoon dog (Nyctereutes procyonoides, Gray 1834): applied perspective to common farming practices. PhD Dissertation, University of Kuopio, FinlandGoogle Scholar
  32. Korhonen H, Harri M, Asikainen J (1982) Effect of various diets and energy levels on the growth of farmed raccoon dogs. Savonia 5:1–9Google Scholar
  33. LeBlanc PJ, Obbard M, Battersby BJ, Felskie AK, Brown L, Wright PA, Ballantyne JS (2001) Correlations of plasma lipid metabolites with hibernation and lactation in wild black bears Ursus americanus. J Comp Physiol B 171:327–334CrossRefPubMedGoogle Scholar
  34. Levinsky NG, Berliner RW (1959) Changes in composition of the urine in ureter and bladder at low urine flow. Am J Physiol 196:549–553Google Scholar
  35. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  36. Lundberg DA, Nelson RA, Wahner HW, Jones JD (1976) Protein metabolism in the black bear before and during hibernation. Mayo Clin Proc 51:716–722PubMedGoogle Scholar
  37. Mathews CK, Holde KE van (1996) Biochemistry, 2nd edn. Benjamin/Cummings, Menlo Park, CAGoogle Scholar
  38. Miller BM, Cersosimo E, McRae J, Williams PE, Lacy WW, Abumrad NN (1983) Interorgan relationships of alanine and glutamine during fasting in the conscious dog. J Surg Res 35:310–318PubMedGoogle Scholar
  39. Nelson RA (1980) Protein and fat metabolism in hibernating bears. Fed Proc 39:2955–2958PubMedGoogle Scholar
  40. Nelson RA, Wahner HW, Jones JD, Ellefson RD, Zollman PE (1973) Metabolism of bears before, during, and after winter sleep. Am J Physiol 224:491–496PubMedGoogle Scholar
  41. Nelson RA, Jones JD, Wahner HW, McGill DB, Code CF (1975) Nitrogen metabolism in bears: urea metabolism in summer starvation and in winter sleep and role of urinary bladder in water and nitrogen conservation. Mayo Clin Proc 50:141–146PubMedGoogle Scholar
  42. Nelson RA, Steiger DL, Beck TDI (1983) Neuroendocrine and metabolic interactions in the hibernating black bear. Acta Zool Fenn 174:137–141Google Scholar
  43. Nelson RA, Beck TDI, Steiger DL (1984) Ratio of serum urea to serum creatinine in wild black bears. Science 226:841–842PubMedGoogle Scholar
  44. Nieminen P, Käkelä R, Mustonen A-M, Hyvärinen H, Asikainen J (2001) Exogenous melatonin affects lipids and enzyme activities in mink (Mustela vison) liver. Comp Biochem Physiol C 128:203–211CrossRefGoogle Scholar
  45. Nieminen P, Mustonen A-M, Asikainen J, Hyvärinen H (2002) Seasonal weight regulation of the raccoon dog (Nyctereutes procyonoides): interactions between melatonin, leptin, ghrelin, and growth hormone. J Biol Rhythms 17:155–163PubMedGoogle Scholar
  46. Palumbo PJ, Wellik DL, Bagley NA, Nelson RA (1983) Insulin and glucagon responses in the hibernating black bear. Int Conf Bear Res Manage 5:291–296Google Scholar
  47. Reidy SP, Weber J-M (2000) Leptin: an essential regulator of lipid metabolism. Comp Biochem Physiol A 125:285–297CrossRefGoogle Scholar
  48. Richelsen B (1997) Action of growth hormone in adipose tissue. Horm Res 48 (Suppl 5):105–110PubMedGoogle Scholar
  49. Rothwell NJ, Saville ME, Stock MJ (1983) Role of insulin in thermogenic responses to refeeding in 3-day-fasted rats. Am J Physiol 245:E160–E165PubMedGoogle Scholar
  50. Siivonen L (1972) The raccoon dog (in Finnish). In: Siivonen L (ed) Mammals in Finland 2. Otava, Keuruu, Finland, pp 140–148Google Scholar
  51. Tveit B, Larsen F (1983) Suppression and stimulation of TSH and thyroid hormones in bulls during starvation and refeeding. Acta Endocrinol 103:223–226PubMedGoogle Scholar
  52. Watts P, Cuyler C (1988) Metabolism of the black bear under simulated denning conditions. Acta Physiol Scand 134:149–152PubMedGoogle Scholar
  53. Wolfe RR, Nelson RA, Stein TP, Rogers L, Wolfe MH (1982) Urea nitrogen reutilization in hibernating bears (Abstract). Fed Proc 41:1623Google Scholar
  54. Xiao Y (1996) Seasonal testicular and moulting cycles in the adult male raccoon dog (Nyctereutes procyonoides) and the effects of melatonin implants. PhD Dissertation, Kuopio University Publications C, Natural and Environmental Sciences 39, University of Kuopio, FinlandGoogle Scholar
  55. Young VR, Munro HN (1978) Nτ-methylhistidine (3-methylhistidine) and muscle protein turnover: an overview. Fed Proc 37:2291–2300PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • A.-M. Mustonen
    • 1
  • P. Nieminen
    • 1
  • M. Puukka
    • 2
  • J. Asikainen
    • 1
  • S. Saarela
    • 3
  • S.-L. Karonen
    • 4
  • J. V. K. Kukkonen
    • 1
  • H. Hyvärinen
    • 1
  1. 1.Department of BiologyUniversity of JoensuuJoensuuFinland
  2. 2.Department of Clinical ChemistryUniversity of OuluOuluFinland
  3. 3.Department of BiologyUniversity of OuluOuluFinland
  4. 4.Department of Clinical ChemistryBiomedicum HelsinkiHelsinkiFinland

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