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Role of Photoperiod During Seasonal Acclimation in Winter-Active Small Mammals

  • Chapter
Environmental Signal Processing and Adaptation

Abstract

Small mammals living in moderate or arctic climatic zones regularly experience seasonal changes in temperature and food availability. Ambient temperatures during winter are well below the thermoneutral zone of small mammals (15–30°C), and food is available only as a fraction of food availability during summer. Despite such unfavorable conditions, small mammals exploit habitats close to or even beyond the arctic circle [18, 51, 55]. Winter can be considered as a seasonal bottleneck for small mammals, causing pressure for the evolution of seasonal acclimation. An entire scope of behavioral and physiological adjustments is used for seasonal acclimation, which may include cessation of reproduction, reduction of body mass, improvements of fur insulation, and the occurrence of daily torpor or hibernation in the winter season. These measures can be used to reduce individual energy requirements during winter [32, 108]. On the other hand, the low ambient temperature in winter also demands improvements in cold tolerance in small mammals when they remain active during winter. This can be achieved by better insulation of winter fur as well as improvements in their capacity for thermoregulatory heat production. Thermal insulation of fur largely depends of the thickness of the air layer trapped in the fur. Small mammals have only a small capacity to increase the thickness of their fur and therefore have only a very limited possibility of seasonal improvement of thermal insulation [29, 43]. They have to rely on their capacity for heat production in order to maintain a high body temperature. Seasonal acclimation therefore appears a difficult task where small mammals have to solve a rather paradoxical situation, they have to exploit measures for reduction of their individual energy expenses, and at the same time to create a greater potential of energy dissipation for thermoregulation.

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References

  1. Bartness TJ, Elliott JA, Goldman BD (1989) Control of torpor and body weight patterns by a seasonal timer in Siberian hamsters. Am J Physiol 257: R142–R149

    PubMed  CAS  Google Scholar 

  2. Bartness TJ, Wade GN (1984) Photoperiodic control of body weight and energy metabolism in Syrian hamsters (Mesocricetus auratus): role of pineal gland, melatonin, gonads, and diet. Endocrinology 114:492–498

    Article  PubMed  CAS  Google Scholar 

  3. Bienengraeber M, Echtay KS, Klingenberg M (1998) H+ transport by uncoupling protein (UCP-1) Is dependent on a histidine pair, absent in UCP-2 and UCP-3. Biochemistry 37:3–8

    Article  PubMed  CAS  Google Scholar 

  4. Bligh J (1966) The thermosensitivity of the hypothalamus and thermoregulation in mammals. Biol Rev 41:317–367

    Article  PubMed  CAS  Google Scholar 

  5. Boss O, Samec S, Kuhne F, Bijlenga P, Assimacopoulosjeannet F, Seydoux J, Giacobino JP, Muzzin P (1998) Uncoupling protein-3 expression in rodent skeletal muscle is modulated by food intake but not by changes in environmental temperature. J Biol Chem273:5–8

    Google Scholar 

  6. Boss O, Samec S, Paolonigiacobino A, Rossier C, Dulloo AG, Seydoux J, Muzzin P, Giacobino JP (1997) Uncoupling protein-3: a new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett 408:39–42

    Article  PubMed  CAS  Google Scholar 

  7. Bouillaud F, Ricquier D, Mory G, Thibault J (1984) Increased level of mRNA for the uncoupling protein in brown adipose tissue of rats during thermogenesis induced by cold exposure or norepinephrine infusion. J Biol Chem 259:11583–11586

    PubMed  CAS  Google Scholar 

  8. Böckler H, Heldmaier G (1983) Interaction of shivering and non-shivering thermogenesis during cold exposure in seasonally-acclimatized Djungarian hamsters (Phodopus sungorus). J Therm Biol 8:97–98

    Article  Google Scholar 

  9. Brück K, Wünnenberg W (1966) Beziehung zwischen Thermogenese im “braunen” Fettgewebe, Temperatur im cervicalen Anteil des Vertebralkanals und Kältezittern. Pflügers Arch 290:167–183

    Article  Google Scholar 

  10. Buchberger A, Heldmaier G, Steinlechner S, Latteier B (1983) Photoperiod and temperature effects on adrenal tyrosine hydroxylase and its relation to nonshivering thermogenesis. Pflügers Arch 399:79–82

    Article  PubMed  CAS  Google Scholar 

  11. Cannon B, Nedergaard J, Sundin U (1981) Thermogenesis, brown fat and thermogenin. Elsevier North Holland, Amsterdam, pp 99–120

    Google Scholar 

  12. Deboer T, Tobler I (1994) Sleep EEG after daily torpor in the Djungarian hamster: similarity to the effects of sleep deprivation. Neurosci Lett 166:35–38

    Article  PubMed  CAS  Google Scholar 

  13. Dehnel A (1949) Studies on the genus Sorex l. Ann Univ Mariae Curie-Sklodowska Lublin-Polonia IV,2:18–104

    Google Scholar 

  14. Depocas F (1960) The calorigenic response of cold-acclimated white rats to infused noradrenaline. Can J Biochem Physiol 38:107–114

    Article  PubMed  CAS  Google Scholar 

  15. Desautels M, Dulos RA (1988) Is adrenergic innervation essential for maintenance of UCP in hamster BAT mitochondria? Am J Physiol 254: R1035–R1042

    PubMed  CAS  Google Scholar 

  16. Feist DD, Feist CF (1986) Effects of cold, short day and melatonin on thermogenesis, body weight and reproductive organs in Alaskan red-backed voles. J Comp Physiol B 156:741–746

    Article  PubMed  CAS  Google Scholar 

  17. Feist DD, Morrison PR (1981) Seasonal changes in metabolic capacity and norepinephrine thermogenesis in the Alaskan red-backed vole: environmental cues and annual differences. Comp Biochem Physiol 69A: 697–700

    Article  Google Scholar 

  18. Feist DD, Rosenmann M (1976) Norepinephrine thermogenesis in seasonally acclimatized and cold acclimated red-backed voles in Alaska. Can J Physiol Pharmacol 54: 146–153

    Article  PubMed  CAS  Google Scholar 

  19. Figala J, Hoffmann K, Goldau G (1973) Zur Jahresperiodik beim Dsungarischen Zwerghamster Phodopus sungorus Pallas. Oecologia 12:89–118

    Article  Google Scholar 

  20. Flaim KE, Horowitz JM, Horwitz BA (1976) Functional and anatomical characteristics of the nerve-brown adipose interaction in the rat. Pflügers Arch 365:9–14

    Article  PubMed  CAS  Google Scholar 

  21. Fleury C, Neverova M, Collins S, Raimbault S, Champigny O, Levimeyrueis O, Bouillaud F, Seldin MF, Surwit RS, Ricquier D, Warden CH (1997) Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat Genet 15:269–272

    Article  PubMed  CAS  Google Scholar 

  22. Foster DO, Frydman ML (1978) Nonshivering thermogenesis in the rat. II. Measurements of blood flow with microspheres point to brown adipose tissue as the dominant site of the calorigenesis induced by noradren. Can J Physiol Pharmacol 56:110–122

    Article  PubMed  CAS  Google Scholar 

  23. Geiser F (1987) Hibernation and daily torpor in two pygmy possums (Cercartetus spp., Marsupialia). Physiol Zool 60:93–102

    Google Scholar 

  24. Haim A (1982) Effects of long scotophase and cold acclimation on heat production in two diurnal rodents. J Comp Physiol 148:77–81

    Google Scholar 

  25. Haim A, Fourie FR (1980) Heat production in cold and long scotophase acclimated and winter acclimatized rodents. Int J Biometeorol 24:231–236

    Article  PubMed  CAS  Google Scholar 

  26. Haim A, Yahav S (1982) Non-shivering thermogenesis in winter-acclimatized and in long-scotophase and cold-acclimated Apodemus Mystacinus (Rodentia). J Therm Biol 7:193–195

    Article  Google Scholar 

  27. Hainsworth FR, Wolf LL (1970) Regulation of oxygen consumption and body temperature during torpor in a hummingbird, Eulampis jugularis. Science 168:368–369

    Article  PubMed  CAS  Google Scholar 

  28. Halaas JL, Gajiwala KS, Maffei M, Cohen SL, Chait BT, Rabinowitz D, Lallone RL, Burley SK, Friedman JM (1995) Weight-reducing effects of the plasma protein encoded by the obese gene. Science. 269:543–546

    Article  PubMed  CAS  Google Scholar 

  29. Hart JS (1965) Seasonal changes in insulation of the fur. Can J Zool 34:53–57

    Article  Google Scholar 

  30. Hartung TG, Dewsbury DA (1979) Nest building behavior in seven species of muroid rodents. Behav Neural Biol 27:532–539

    Article  Google Scholar 

  31. Heldmaier G (1971) Zitterfreie Wärmebildung und Körpergrösse bei Säugetieren. Z Vergl Physiol 73:222–248

    Article  Google Scholar 

  32. Heldmaier G (1989) Seasonal acclimization of energy requirements in mammals: functional significance of body weight control, hypothermia, torpor and hibernation. In: Wieser W, Gnaiger E (eds) Energy Transformations in Cells and Organisms. Georg Thieme, Stuttgart, pp 130–139

    Google Scholar 

  33. Heldmaier G, Böckler H, Buchberger A, Klaus S, Puchalski W, Steinlechner S, Wiesinger H (1986) Seasonal variation of thermogenesis. In: Heller HC, Musacchia XJ, Wang LCH (eds) Living in the cold: physiological and biochemical adaptations, Elsevier, New York, p. 361–372

    Google Scholar 

  34. Heldmaier G, Buchberger A (1985) Sources of heat during nonshivering thermogenesis in Djungarian hamsters: a dominant role of brown adipose tissue during cold adaptation. J Comp Physiol B 156:237–245

    Article  PubMed  CAS  Google Scholar 

  35. Heldmaier G, Jablonka B (1985) Seasonal differences in thermogenic adaptation evoked by daily injection of noradrenaline. J Therm Biol 10:97–99

    Article  CAS  Google Scholar 

  36. Heldmaier G, Klaus S, Wiesinger H (1990) Seasonal adaptation of thermoregulatory heat production in small mammals. In: Bligh J, Voigt K (eds) Thermoreception and temperature regulation, Springer, Berlin Heidelberg New York, pp 235–243

    Chapter  Google Scholar 

  37. Heldmaier G, Klaus S, Wiesinger H, Friedrichs U, Wenzel M (1989) Cold acclimation and thermogenesis. In: Malan A, Canguilhem B (eds) Living in the cold II, John Libbey Eurotext, Paris, pp 347–358

    Google Scholar 

  38. Heldmaier G, Klingenspor M, Werneyer M, Lampi BJ, Brooks SP, Storey KB Metabolic adjustments during daily torpor in the Djungarian hamster. Am. J. Physiol. 276: E896-906

    Google Scholar 

  39. Heldmaier G, Lynch GR (1986) Pineal involvement in thermoregulation and acclimatization. Pineal Res. Rev. 4:97–139

    CAS  Google Scholar 

  40. Heldmaier G, Ortmann S, Körtner G (1993) Energy requirements of hibernating alpine marmots. In: Carey C, Florant GL, Wunder BA, Horwitz BA (eds). Life in the cold: ecological, physiological and molecular mechanisms, Westview Press, Boulder, pp 175–183

    Google Scholar 

  41. Heldmaier G, Seidl K (1985) Plasma free fatty acid levels during cold-induced and nor-adrenaline-induced nonshivering thermogenesis in the Djungarian hamster. J Comp Physiol B 155:679–684

    Article  PubMed  CAS  Google Scholar 

  42. Heldmaier G, Steiger R, Ruf TP (1993). Suppression of Metabolic Rate in Hibernation. In: Carey C, Florant GL, Wunder BA, Horwitz BA (eds) Life in the cold, Westview Press, Boulder, pp 545–548

    Google Scholar 

  43. Heldmaier G, Steinlechner S (1981) Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopus sungorus), living in natural photoperiod. J Comp Physiol 142:429–437

    Google Scholar 

  44. Heldmaier G, Steinlechner S (1981) Seasonal pattern and energetics of short daily torpor in the Djungarian hamster, Phodopus sungorus. Oecologia 48:265–270

    Article  Google Scholar 

  45. Heldmaier G, Steinlechner S, Rafael J (1982) Nonshivering thermogenesis and cold resistance during seasonal acclimatization in the Djungarian hamster. J Comp Physiol 149:1–9

    Google Scholar 

  46. Heldmaier G, Steinlechner S, Rafael J, Latteier B (1982) Photoperiod and ambient temperature as environmental cues for seasonal thermogenic adaptation in the Djungarian hamster, Phodopus sungorus. Int J Biometeorol 26:339–345

    Article  PubMed  CAS  Google Scholar 

  47. Heldmaier G, Steinlechner S, Rafael J, Vsiansky P (1981) Photoperiodic control and effects of melatonin on nonshivering thermogenesis and brown adipose tissue. Science 212:917–919

    Article  PubMed  CAS  Google Scholar 

  48. Heldmaier G, Steinlechner S, Ruf TP, Wiesinger H, Klingenspor M (1989) Photoperiod and thermoregulation in vertebrates: body temperature rhythms and thermogenic acclimation. J Biol Rhythms 4:251–265

    Article  PubMed  CAS  Google Scholar 

  49. Himms-Hagen, J. (1984) Nonshivering thermogenesis. Brain Res Bull 12:151–160

    Article  PubMed  CAS  Google Scholar 

  50. Hudson JW (1978) Shallow, daily torpor: a thermoregulatory adaptation. In: Wang LCH, Hudson JW (eds) Strategies in cold: natural torpidity and thermogenesis. Academic Press, New York, pp 67–108

    Google Scholar 

  51. Hyvärinen H, Heikura K (1971) Effects of age and seasonal rhythm on the growth patterns of some small mammals in Finland and in Kirkenes, Norway. J Zool Lond 165:545–556

    Article  Google Scholar 

  52. Jacobsson A, Nedergaard J, Cannon B (1986) Alpha-and beta-adrenergic control of thermogenin mRNA expression in brown adipose tissue. Biosci Rep 6:621–631

    Article  PubMed  CAS  Google Scholar 

  53. Jannett JF (1984) Reproduction of the montane vole, Microtus montanus, in subnivean populations. In: Merritt JF (ed) Winter ecology of small mammals, Carnegie Museum of Natural History, Pittsburgh, pp 215–224

    Google Scholar 

  54. Jansky L (1973) Non-shivering thermogenesis and its thermoregulatory significance. Biol Rev 48:85–132

    PubMed  CAS  Google Scholar 

  55. Kaikusalo A, Test J (1984) Winter Breeding of Microtine Rodents a Kilpisjärvi, Finnish Lapland. In: Merritt JF (ed) Winter ecology of small mammals, Carnegie Museum of Natural History, Pittsburgh, pp 243–252

    Google Scholar 

  56. King JA, Maas D, Weismann RG (1964) Geographic variation in nest size among species of Peromyscus. Evolution 18:230–234

    Article  Google Scholar 

  57. Klaus S (1991) Development of Phodopus sungorus brown preadipocytes in primary cell culture: effect of an atypical beta-adrenergic agonist, insulin and triiodothyronin on differentiation, mitochondrial development and expression of the uncoupling protein UCP. J Cell Biol 115:1783–1790

    Article  PubMed  CAS  Google Scholar 

  58. Klaus S, Casteilla L, Bouillaud F, Ricquier D (1991) Minireview: the uncoupling protein UCP: a mambraneous mitochondrial ion carrier exclusively expressed in brown adipose tissue. Int J Biochem 23(9): 791–801

    Article  PubMed  CAS  Google Scholar 

  59. Klaus S, Heldmaier G, Ricquier D (1988) Seasonal acclimation of bank voles and wood mice: nonshivering thermogenesis and thermogenic properties of brown adipose tissue mitochondria. J Comp Physiol 158:157–164

    CAS  Google Scholar 

  60. Klingenspor M, Dickopp A, Heldmaier G, Klaus S (1996) Short photoperiod reduces leptin gene expression in white and brown adipose tissue of Djungarian hamsters. FEBS. Lett. 399:290–294

    Article  PubMed  CAS  Google Scholar 

  61. Klingenspor M, Ebbinghaus C, Hulshorst G, Stöhr S, Spiegelhalter F, Haas K, Heldmaier G (1996) Multiple regulatory steps are involved in the control of lipoprotein lipase activity in brown adipose tissue. J. Lipid. Res. 37:1685–1695

    PubMed  CAS  Google Scholar 

  62. Klingenspor M, Klaus S, Wiesinger H, Heldmaier G (1989) Short photoperiod and cold activate brown fat lipoprotein lipase in the Djungarian hamster. Am. J. Physiol. 257: R1123-7

    Google Scholar 

  63. Klingenspor M, Meywirth A, Stöhr S, Heldmaier G (1994) Effect of unilateral surgical denervation of brown adipose tissue on uncoupling protein mRNA level and cytochrome-c-oxidase activity in the Djungarian hamster. J Comp Physiol B 664–670

    Google Scholar 

  64. Klingenspor M, Niggemann H, Heldmaier G (2000) Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian Hamster, Phodopus sungorus. J Comp Physiol B 170:37–43

    Article  PubMed  CAS  Google Scholar 

  65. Kulzer E (1965) Temperaturregulation bei Fledermäusen (Chiroptera) aus verschiedenen Klimazonen. Z Vergl Physiol 50:1–34

    Article  Google Scholar 

  66. Kuusela P, Jacobsson A, Klingenspor M, Rehnmark S, Heldmaier G, Cannon B, Nedergaard J (1997) Contrasting adrenergic effects on lipoprotein lipase gene expression in the brown adipose tissue of intact mice and in cultured brown adipocytes from mice. BBA Lipid Metab 1345:327–337

    Article  CAS  Google Scholar 

  67. Layne JN (1969) Nest-building behavior in three species of deer mice, Peromyscus. Behaviour 35:288–303

    Article  Google Scholar 

  68. Lynch GR (1973) Seasonal changes in thermogenesis, organ weights, and body composition in the white-footed mouse, Peromyscus leucopus. Oecologia 13:363–376

    Article  Google Scholar 

  69. Lynch GR (1973) Effect of simultaneous exposure to differences in photoperiod and temperature on the seasonal molt and reproductive system of the white-footed mouse, Persomyscus leucopus. Comp Biochem Physiol 44A: 1373–1376

    Article  Google Scholar 

  70. Lynch GR, Sullivan JK, Gendler SL (1980). Temperature regulation in the mouse, Peromyscus leucopus: effects of various photoperiods, pinealectomy and melatonin administration. Int J Biometeorol 24:49–55

    Article  PubMed  CAS  Google Scholar 

  71. Lynch GR, Vogt DF, Smith HR (1978) Seasonal study of spontaneous daily torpor in the white-footed mouse, Peromyscus leucopus. Physiol Zool 51:289–299

    Google Scholar 

  72. Maier HA, Feist DD (1991) Thermoregulation, growth, and reproduction in Alaskan collared lemmings — role of short day and cold. Am J Physiol 261: R522-530

    Google Scholar 

  73. Mcdevitt RM, Speakman JR (1996) Summer acclimatization in the short tailed field vole, Microtus agrestis. J Comp Physiol B 166:286–293

    Article  PubMed  CAS  Google Scholar 

  74. Mercer J.G, Moar KM, Rayner DV, Trayhurn P, Hoggard N (1997) Regulation of leptin receptor and NPY gene expression in hypothalamus of leptin-treated obese (ob/ob) and cold-exposed lean mice. FEBS Lett 402:185–188

    Article  PubMed  CAS  Google Scholar 

  75. Meywirth A, Redlin U, Steinlechner S, Heldmaier G (1990) Role of the sympathetic innervation in the cold-induced activation of 5x-deiodinase in brown adipose tissue of the Djungarian hamster. Can J Physiol Pharmacol 69:1896–1900

    Article  Google Scholar 

  76. Mitchell P, Moyle J (1967) Respiration driven proton translocation in rat liver mitochondria. Biochem J 104:588–600

    PubMed  CAS  Google Scholar 

  77. Mrosovsky N, Fisher KC (1970) Sliding set points for body weight in ground squirrels during the hibernation season. Can J Zool 48:241–247

    Article  PubMed  CAS  Google Scholar 

  78. Nicholls DG, Locke RM (1984) Thermogenic mechanisms in brown fat: physiological reviews. Am Physiol Soc 1–64

    Google Scholar 

  79. Niethammer J (1956) Das Gewicht der Waldspitzmaus Sorex araneus (Linne 1758) im Jahresverlauf. Säugetierk Mitt 160–165

    Google Scholar 

  80. Ortmann S, Heldmaier G (1997) Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschaften 84:28–32

    Article  PubMed  CAS  Google Scholar 

  81. Park IRA, Himms-Hagen J (1988) Neural influences on tropic changes in brown adipose tissue during cold acclimation. Am J Physiol 255: R874–R881

    PubMed  CAS  Google Scholar 

  82. Pelleymounter MA, Cullen MJ, Baker MB, Hecht R, Winters D, Boone T, Collins F (1995) Effects of the obese gene product on body weight regulation in ob/ob mice. Science 269:540–543

    Article  PubMed  CAS  Google Scholar 

  83. Puchalski W, Böckler H, Heldmaier G, Langefeld M (1987) Organ blood flow and brown adipose tissue oxygen consumption during noradrenaline-induced nonshivering thermogenesis in the Djungarian hamster. J Exp Zool 242:263–271

    Article  PubMed  CAS  Google Scholar 

  84. Puchalski W, Bulova SJ, Lynch CB, Lynch GR (1988) Photoperiod, temperature and melatonin effects on thermoregulatory effects on thermoregulatory behavior in Djungarian hamsters. Physiol Behav 42:173–177

    Article  PubMed  CAS  Google Scholar 

  85. Rafael J, Vsiansky P, Heldmaier G (1985) Seasonal adaptation of brown adipose tissue in the Djungarian hamster. J Comp Physiol 155:521–528

    CAS  Google Scholar 

  86. Reddy AB, Cronin AS, Ford H, Ebling FJ (1999) Seasonal regulation of food intake and body weight in the male Siberian hamster: studies of hypothalamic orexin (hypocretin), neuropeptide Y(NPY) and pro-opiomelanocortin (POMC). Eur J Neurosci 11:3255–3264

    Article  PubMed  CAS  Google Scholar 

  87. Rehnmark S, Nechad M, Herron D, Cannon B, Nedergaard J (1990) Alpha-and betaadrenergic induction of the expression of the uncoupling protein thermogenin in brown adipocytes differentiated in culture. J Biol Chem 265:16464–16471

    PubMed  CAS  Google Scholar 

  88. Rosenmann M, Morrison P, Feist D (1975) Seasonal changes in the metabolic capacity of red-backed voles. Physiol Zool 48:303–310

    Google Scholar 

  89. Ruby NF, Ibuka N, Barnes BM, Zucker I (1989) Suprachiasmatic nuclei influence torpor and circadian temperature rhythms in hamsters. Am J Physiol 257: R210–R215

    PubMed  CAS  Google Scholar 

  90. Ruby NF, Nelson RJ, Licht P, Zucker I (1993) Prolactin and testosterone inhibit torpor in Siberian hamster. Am J Physiol 264: R123–R128

    PubMed  CAS  Google Scholar 

  91. Ruby NF, Zucker I (1992). Daily torpor in the absence of the suprachiasmatic nucleus in Siberian hamster. Am J Physiol 263: R353-R362

    Google Scholar 

  92. Ruf TP, Heldmaier G (1992) Reduced locomotor activity following daily torpor in the Djungarian hamster: recovery from hypothermia? Naturwissenschaften 79:574–575

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  94. Ruf TP, Heldmaier G (1993) Individual energetic strategies in winter-adapted Djungarian hamsters The relation between daily torpor, locomotion, and food consumption. In: Carey C, Florant GL, Wunder BA, Horwitz BA (eds). Life in the cold: ecological, physiological and molecular mechanisms, Westview Press, Boulder, pp 99–107

    Google Scholar 

  95. Ruf TP, Klingenspor M, Preis H, Heldmaier G (1991) Daily torpor in the Djungarian hamster (Phodopus sungorus): interactions with food intake, activity, and social behaviour. J Comp Physiol B 160:609–615

    Article  Google Scholar 

  96. Ruf TP, Stieglitz A, Steinlechner S, Blank JL, Heldmaier G (1993) Cold exposure and food restriction facilitate physiological responses to short photoperiod in Djungarian hamsters (Phodopus sungorus). J Exp Zool 267:104–112

    Article  PubMed  CAS  Google Scholar 

  97. Seydoux J, Tribollet E, Stadelmann A, Girardier L (1984) Effectiveness of surgical denervation of interscapular brown adipose tissue in the rat: further observations. In: Hales JRS (ed) Thermal physiology, Raven Press, New York, pp 197–199

    Google Scholar 

  98. Steinlechner S, Heldmaier G (1982) Role of photoperiod and melatonin in seasonal acclimatization of the Djungarian hamster, Phodopus sungorus. Int J Biometeorol 26: 329–337

    Article  PubMed  CAS  Google Scholar 

  99. Steinlechner S, Heldmaier G, Becker H (1983) The seasonal cycle of body weight in the Djungarian hamster: photoperiod control and the influence of starvation and melatonin. Oecologia 60:401–405

    Article  Google Scholar 

  100. Steinlechner S, Heldmaier G, Weber C, Ruf TP (1986) Role of photoperiodic: pineal gland interaction in torpor control. In: Heller HC, Musacchia XJ, Wang LCH (eds) Living in the cold: physiological and biochemical adaptations, Elsevier, New York, pp 301–308

    Google Scholar 

  101. Stieglitz A, Spiegelhalter F, Klante G, Heldmaier G (1995). Urinary 6-sulphatoxymelatonin excretion reflects pineal melatonin secretion in the Djungarian hamster (Phodopus sungorus). J Pineal Res 18:69–76

    Article  PubMed  CAS  Google Scholar 

  102. Szelenyi Z, Zeisberger E, Brück K (1976) Effects of electrical stimulation in the lower brainstem on temperature regulation in the unanaesthetized guinea-pig. Pflügers Arch 364:123–127

    Article  PubMed  CAS  Google Scholar 

  103. Vitale PM, Darrow JM, Duncan MJ, Shustak CA, Goldman BD (1985) Effects of photperiod, pinealectomy and castration on body weight and daily torpor in Djungarian hamsters (Phodopus sungorus). J Endocrinol 106:367–375

    Article  PubMed  CAS  Google Scholar 

  104. Weiner J (1987) Limits to energy budget and tactics in energy investments during reproduction in the Djungarian Hamster. Symp Zool Soc Lond 57:167–187

    Google Scholar 

  105. Wiesinger H, Heldmaier G, Buchberger A (1989) Effect of photoperiod and acclimation temperature on non-shivering thermogenesis and GDP-binding of brown fat mitochondria in the Djungarian hamster Phodopus s. sungorus. Pflügers Arch 413:667–672

    Article  PubMed  CAS  Google Scholar 

  106. Wiesinger H, Klaus S, Heldmaier G, Champigny O, Ricquier D (1990) Increased nonshivering thermogenesis, brown fat cytochrome-c oxidase activity, GDP binding, and uncoupling protein mRNA levels after short daily cold exposure of Phodopus sungorus. Can J Physiol Pharmacol 68:195–200

    Article  PubMed  CAS  Google Scholar 

  107. Wolfe JL (1970) Experiments on nest-building behaviour in Peromyscus (Rodentia:Cricetinae). Anim Behav 18:613–615

    Article  Google Scholar 

  108. Wunder BA (1984) Strategies for and environmental cueing mechanisms of seasonal changes in thermoregulatory parameters of small mammals. Carnegie Mus Nat Hist Spec Publ 1–21

    Google Scholar 

  109. Wunder BA, Dobkin DS, Gettinger RD (1977) Shifts of thermogenesis in the prairie vole (Microtus ochrogaster). Oecologia 29:11–26

    Article  Google Scholar 

  110. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue [published erratum appears in Nature 1995 Mar 30; 374(652):479] [see comments]. Nature 372:425–432

    Article  PubMed  CAS  Google Scholar 

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  1. Gerhard Heldmaier and Martin Klingenspor Department of Biology, Philipps-University, D-35032, Marburg, Germany

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Heldmaier, G., Klingenspor, M. (2003). Role of Photoperiod During Seasonal Acclimation in Winter-Active Small Mammals. In: Heldmaier, G., Werner, D. (eds) Environmental Signal Processing and Adaptation. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-56096-5_12

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  • DOI: https://doi.org/10.1007/978-3-642-56096-5_12

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-62858-0

  • Online ISBN: 978-3-642-56096-5

  • eBook Packages: Springer Book Archive

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