Abstract
The Malagasy primate Cheirogaleus medius hibernates in tree holes for 7 months, although ambient temperatures during hibernation rise above 30°C in their natural environment. In a field study we show that during hibernation the body temperature of most lemurs fluctuates between about 10°C and 30°C, closely tracking the diurnal fluctuations of ambient temperature passively. These lemurs do not interrupt hibernation by spontaneous arousals, previously thought to be obligatory for all mammalian hibernators. However, some lemurs hibernate in large trees, which provide better thermal insulation. Their body temperature fluctuates only little around 25°C, but they show regular arousals, as known from temperate and arctic hibernators. The results from this study demonstrate that maximum body temperature is a key factor necessitating the occurrence of arousals. Furthermore, we show that hibernation is not necessarily coupled to low body temperature and, therefore, low body temperature should no longer be included in the definition of hibernation.
Similar content being viewed by others
Abbreviations
- T a :
-
Ambient temperature
- T b :
-
Body temperature
- T h :
-
Tree hole temperature
References
Armitage KB (1979) Food selectivity by yellow-bellied marmots. J Mammal 60:628–629
Arnold W, Heldmaier G, Ortmann S, Pohl H, Ruf TP, Steinlechner S (1991) Ambient temperatures in hibernacula and their energetic consequences for alpine marmots (Marmota marmota). J Therm Biol 16:223–226
Barnes BM, Kretzmann M, Licht P, Zucker I (1986) The influence of hibernation on testis growth and spermatogenesis in the golden-mantled ground squirrel, Spermophilus lateralis. Biol Reprod 35:1289–1297
Bartels W, Law BS, Geiser F (1998) Daily torpor and energetics in a tropical mammal, the northern blossom-bat Macroglossus minimus (Megachiroptera). J Comp Physiol B 168:233–239
Buck CL, Barnes BM (1999) Temperatures of hibernacula and changes in body composition of arctic ground squirrels over winter. J Mammal 80:1264–1276
Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181
Cossins AR, Barnes B (1996) Southern discomfort. Nature 382:582–583
Daan S, Barnes BM, Strijkstra AM (1991) Warming up for sleep?—ground squirrels sleep during arousals from hibernation. Neurosci Lett 128:265–268
Dausmann KH (2005) Measuring body temperature in the field—evaluation of external vs. implanted transmitters in a small mammal. J Therm Biol (in press)
Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429:825–826
Fietz J (1999) Monogamy as a rule rather than exception in nocturnal lemurs: the case of the fat-tailed dwarf lemur, Cheirogaleus medius. Ethology 105:259–272
Fietz J, Ganzhorn JU (1999) Feeding ecology of the hibernating primate Cheirogaleus medius: how does it get so fat? Oecologia 121:157–164
Fietz J, Tataruch F, Dausmann KH, Ganzhorn JU (2003) White adipose tissue composition in the free-ranging fat-tailed dwarf lemur (Cheirogaleus medius; Primates), a tropical hibernator. J Comp Physiol B 173:1–10
Frank CL, Storey KB (1995) The optimal depot fat composition for hibernation by golden-mantled ground-squirrels (Spermophilus lateralis). J Comp Physiol B 164:536–542
Ganzhorn JU, Sorg J-P (eds) (1996) Ecology and economy of a tropical dry forest in Madagascar. Primate Report 46–1
Geiser F, Drury DR (2003) Radiant heat affects thermoregulation and energy expenditure during rewarming from torpor. J Comp Physiol B 173:55–60
Geiser F, Kenagy GJ (1987) Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator. Am J Physiol 252:R897–R901
Geiser F, Ruf TP (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935–966
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 Verlag, Stuttgart, pp 130–139
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
Hladik CM, Charles-Dominique P, Petter JJ (1980) Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A, Petter JJ, Schilling A (eds) Nocturnal Malagasy primates: ecology, physiology and behaviour. Academic, New York, pp 41–73
Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179
Kayser C (1961) The physiology of natural hibernation. Pergamon, Oxford
Lovegrove BG (2003) The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. J Comp Physiol B 173:87–112
Lovegrove BG, Raman J (1998) Torpor patterns in the pouched mouse (Saccostomus campestris; Rodentia): a model animal for unpredictable environments. J Comp Physiol B 168:303–312
Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic, New York
Martin I, Vinas O, Mampel T, Iglesias R, Villarroya F (1993) Effects of cold environment on mitochondrial genome expression in the rat—evidence for a tissue- specific increase in the liver, independent of changes in mitochondrial gene abundance. Biochem J 296:231–234
Müller AE (1999) Social organization of the fat-tailed dwarf lemur (Cheirogaleus medius) in north-western Madagascar. In: Rakotosamimanana B, Rasaminanana H, Ganzhorn JU, Goodman SM (eds) New directions in lemur studies. Kluwer/Plenum, New York, pp 139–157
Mzilikazi N, Lovegrove BG, Ribble DO (2002) Exogenous passive heating during torpor arousal in free-ranging rock elephant shrews, Elephantulus myurus. Oecologia 133:307–314
Ortmann S, Heldmaier G, Schmid J, Ganzhorn JU (1997) Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschaften 84:28–32
Petter JJ (1978) Ecological and physiological adaptations of five sympatric nocturnal lemurs to seasonal variations in food production. In: Chivers DJ, Herbert J (eds) Recent advances in primatology, vol 1. Academic, New York, pp 211–223
Petter-Rousseaux A (1980) Seasonal activity rhythms, reproduction, and body weight variations in five sympatric nocturnal prosimians, in simulated light and climatic conditions. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A, Petter JJ, Schilling A (eds) Nocturnal Malagasy primates: ecology, physiology and behaviour. Academic, New York, pp 137–152
Prendergast BJ, Freeman DA, Zucker I (2002) Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. Am J Physiol Reg I 282:R1054–R1062
Schmid J (2000) Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: energetic consequences and biological significance. Oecologia 123:175–183
Schmid J, Speakman JR (2000) Daily energy expenditure of the grey mouse lemur (Microcebus murinus): a small primate that uses torpor. J Comp Physiol B 170:633–641
Schmid J, Ruf TP, Heldmaier G (2000) Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Mircrocebus myoxinus) in Madagascar. J Comp Physiol B 170:59–68
Strijkstra AM, Hut RA, de Wilde MC, Stieler J, Van der Zee EA (2003) Hippocampal synaptophysin immunoreactivity is reduced during natural hypothermia in ground squirrels. Neurosci Lett 344:29–32
Walter H, Breckle S-W (1986) Spezielle Ökologie der gemäßigten und arktischen Zonen Euro-Nordasiens. Gustav Fischer, Stuttgart
Wang LCH (1979) Time patterns and metabolic rates of natural torpor in the Richardson’s ground squirrel. Can J Zool 57:149–155
Acknowledgements
We are grateful to the Commission Tripartite of the Malagasy Government, the Laboratoire de Primatologie et des Vertébrés de l‘Université d’Antananarivo, the Parc Botanique et Zoologique de Tsimbazaza, the Ministère pour la Production Animale and the Département des Eaux et Forêts for permits to work in Madagascar. We also thank the Centre de Formation Professionnelle Forestière de Morondava for their hospitality and permission to work on their concession. B. Rakotosamimanana, R. Rasoloarison, L. Razafimanantsoa, J. Fietz and J. Schmid supported the field project in numerous ways. We thank the German Primate Centre (DPZ) and P.M. Kappeler for the opportunity to work at the field station. Financial aid from the Deutscher Akademischer Austauschdienst and the Deutsche Forschungsgemeinschaft is gratefully acknowledged. All experiments comply with the current laws of the country where they were performed.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by L.C.-H. Wang
Rights and permissions
About this article
Cite this article
Dausmann, K.H., Glos, J., Ganzhorn, J.U. et al. Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175, 147–155 (2005). https://doi.org/10.1007/s00360-004-0470-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-004-0470-0