, 96:609 | Cite as

Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): a comparison of dry and wet forests

  • J. Schmid
  • J. R. Speakman
Original Paper


Many endotherms save energy during food and water shortage or unpredictable environment using controlled reductions in body temperature and metabolism called torpor. In this study, we measured energy metabolism and water turnover in free-ranging grey mouse lemurs Microcebus murinus (approximately 60 g) using doubly labelled water during the austral winter in the rain forest of southeastern Madagascar. We then compared patterns of thermal biology between grey mouse lemurs from the rain forest and a population from the dry forest. M. murinus from the rain forest, without a distinct dry season, entered daily torpor independent of ambient temperature (T a). There were no differences in torpor occurrence, duration and depth between M. murinus from the rain and dry forest. Mouse lemurs using daily torpor reduced their energy expenditure by 11% in the rain forest and by 10.5% in the dry forest, respectively. There was no significant difference in the mean water flux rates of mouse lemurs remaining normothermic between populations of both sites. In contrast, mean water flux rate of individuals from the dry forest that used torpor was significantly lower than those from the rain forest. This study represents the first account of energy expenditure, water flux and skin temperature (T sk) in free-ranging M. murinus from the rain forest. Our comparative findings suggest that water turnover and therefore water requirement during the austral winter months plays a more restricting role on grey mouse lemurs from the dry forest than on those from the rain forest.


Microcebus murinus Madagascar Doubly labelled water Torpor Water turnover 



daily energy expenditure


mean temperature difference


resting metabolic rate


ambient temperature


skin temperature



We thank the Direction des Eaux et Forêts and the Commission Tripartite for their authorisation to carry out this work. The study has been conducted within the framework of biodiversity assessment studies of the littoral forest fragments initiated by QIT Madagascar Minerals (QMM). J.-B. Ramanamanjato, M. Vincelette and their environmental and conservation team of QMM as well as R. Ernest provided excellent support in the field. We are grateful to Paula Redman and Peter Thomson for technical assistance in the isotope analysis. We thank J. Fietz, J.U. Ganzhorn and three anonymous referees for very helpful comments on the manuscript. This paper is part of the Accord de Collaboration between the Université d’Anananarivo (Départements de Biologie Animale and d’Anthropologie et Biologie Evolutive), QMM and Hamburg University. Financial support from the German Research Foundation (SCHM 1391/2-1, 2-3, 2-4) is gratefully acknowledged. We declare that the experiments complied with the current laws on Madagascar (no. 101–DGDRF/SCB).


  1. 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 114:492–498PubMedGoogle Scholar
  2. Berteaux D, Thomas DW, Bergeron J-M, Lapierre H (1996) Repeatability of daily field metabolic rate in female Meadow Voles (Microtus pennsylvanicus). Funct Ecol 10:751–759CrossRefGoogle Scholar
  3. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181PubMedGoogle Scholar
  4. Corbin GD, Schmid J (1995) Insect secretions determine habitat use patterns by a female lesser mouse lemur (Microcebus murinus). Am J Primatol 37:317–324CrossRefGoogle Scholar
  5. Corp N, Gorman ML, Speakman JR (1997) Ranging behaviour and time budgets of male wood mice Apodemus sylvaticus in different habitats and seasons. Oecologia 109:242–250CrossRefGoogle Scholar
  6. Dausmann KH (2008) Hypometabolism in primates: torpor and hibernation. In: Lovegrove BG, McKechnie AE (eds) Hypometabolism in animals: hibernation, torpor and cryobiology. Interpak Books, Pietermaritzburg, pp 327–336Google Scholar
  7. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2005) Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175:147–155PubMedCrossRefGoogle Scholar
  8. Dewar RE, Wallis JR (1999) Geographical patterning of interannual rainfall variability in the tropics and near tropics: an L-moments approach. J Climate 12:3457–3466CrossRefGoogle Scholar
  9. Downs CT, Perrin MR (1995) The thermal biology of three southern African elephant-shrews. J Therm Biol 20(6):445–450CrossRefGoogle Scholar
  10. Eberle M, Kappeler PM (2004) Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behav Ecol Sociobiol 57:77–90CrossRefGoogle Scholar
  11. Evans M, Green B, Newgrain K (2003) The field energetics and water fluxes of free-living wombats (Marsupialia: Vombatidae). Oecologia 137:171–180PubMedCrossRefGoogle Scholar
  12. Fietz J (1999) Mating system of Microcebus murinus. Am J Primatol 48:127–133PubMedCrossRefGoogle Scholar
  13. Ganzhorn JU, Rohner J-P (1996) Ecology and economy of a tropical dry forest in Madagascar. German Primate Center, GöttingenGoogle Scholar
  14. Ganzhorn JU, Andrianasolo T, Andrianjazalahatra T, Donati G, Fietz J, Lahann P, Ramarokoto REAF, Randriamanga S, Rasarimanana S, Rakotosamimanana B, Ramanamanjato J-B, Randria G, Rasolofoharivelo MT, Razanahoera-Rakototmalala M, Schmid J, Sommer S (2007) Lemurs in Evergreen Littoral Forest Fragments. In: Alonso A (ed) Biodiversity, ecology and conservation of littoral ecosystems in southeastern Madagascar, Tolagnaro (Fort Dauphin). SI/MAB Series, Washington, DC, USA, pp 223–235Google Scholar
  15. Geiser F, Baudinette RV (1988) Daily torpor and thermoregulation in the small dasyurid marsupials Planigale gilesi and Ningaui yvonneae. Aust J Zool 36:473–481CrossRefGoogle Scholar
  16. Geiser F, Coburn DK (1999) Field metabolic rates and water uptake in the blossom-bat Syconycteris australis (Megachiroptera). J Comp Physiol B 169(2):133–138PubMedCrossRefGoogle Scholar
  17. Geiser F, Kenagy GJ (1988) Torpor duration in relation to temperature and metabolism in hibernating ground squirrels. Physiol Zool 61:442–449Google Scholar
  18. Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935–966Google Scholar
  19. Geiser F, Coburn DK, Körtner G, Law BS (1996) Thermoregulation, energy metabolism, and torpor in blossom-bats, Syconycteris australis (Megachiroptera). J Zool 239:583–590CrossRefGoogle Scholar
  20. Genin F, Perret M (2003) Daily hypothermia in captive grey mouse lemurs (Microcebus murinus): effects of photoperiod and food restriction. Comp Biochem Physiol B 136:71–81PubMedCrossRefGoogle Scholar
  21. Green K, Crowley H (1989) Energetics and behaviour of acive subnivean insectivores Antechinus swainsonii and Antechinus stuartii (Marsupialia: Dasyuridae) in the snowy mountains (New South Wales, Australia). Aust Wildl Res 16:509–516CrossRefGoogle Scholar
  22. Heldmaier G (1989) Seasonal acclimazation 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 130–139Google Scholar
  23. Heldmaier G, Ruf T (1992) The impact of daily torpor on energy requirements in the Djungarian hamster, Phodopus sungorus. Physiol Zool 65:994–1010Google Scholar
  24. Hemingway CA, Bynum N (2005) The influence of seasonality on primate diet and ranging. In: Brockman DK, van Schaick CP (eds) Seasonality in primates. Studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge, pp 57–104Google Scholar
  25. Hudson JW (1973) Torpidity in mammals. In: Whittow GC (ed) Comparative physiology of thermoregulation. Academic, London, pp 97–165Google Scholar
  26. Humphries MM, Boutin S, Thomas DW, Ryan JD, Selman C, McAdam AG, Berteaux D, Speakman JR (2005) Expenditure freeze: the metabolic response of small mammals to cold environments. Ecol Lett 8:1326–1333CrossRefGoogle Scholar
  27. Karasov WH (1981) Daily energy expenditure and cost of activity in a free-living mammal. Oecologia 51:253–259CrossRefGoogle Scholar
  28. Körtner G, Geiser F (2009) The key to winter survival: daily torpor in a small arid-zone marsupial. Naturwissenschaften. doi: 10.1007/s00114-008-0492-7
  29. Krol E, Speakman JR (1999) Isotope dilution spaces of mice injected simultaneously with deuterium, tritium and oxygen-18. J Exp Biol 202:2839–2849PubMedGoogle Scholar
  30. Lahann P (2008) Habitat utilization of three sympatric Cheirogaleid lemur species in a littoral rain forest of southeastern Madagascar. Int J Primatol 29:117–134CrossRefGoogle Scholar
  31. Lahann P, Schmid J, Ganzhorn JU (2006) Geographic variation in life history traits of Microcebus murinus in Madagascar. Int J Primatol 27:983–999CrossRefGoogle Scholar
  32. Lifson N, McClintock R (1966) Theory of use of the turnover rates of body water for measuring energy and material balance. J Theor Biol 12:46–74PubMedCrossRefGoogle Scholar
  33. Lovegrove BG (2000a) Daily heterothermy in mammals: coping with unpredictable environments. In: Heldmaier G, Klingenspor M (eds) Life in the cold: 11th International Hibernation Symposium. Springer, Berlin, pp 29–40Google Scholar
  34. Lovegrove BG (2000b) The zoogeography of mammalian basal metabolic rate. Am Nat 156(2):201–219PubMedCrossRefGoogle Scholar
  35. Lovegrove BG, Raman J, Perrin MR (2001) Daily torpor in elephant shrews (Macroscelidea: Elephantulus spp.) in response to food deprivation. J Comp Physiol B 171:11–21PubMedCrossRefGoogle Scholar
  36. Martin RD (1973) A review of the behaviour and ecology of the lesser mouse lemur (Microcebus murinus). In: Crook M (ed) Ecology and behaviour of primates. Acadmic, London, pp 1–68Google Scholar
  37. McDevitt RM, Speakman JR (1994) Central limits to sustainable metabolic-rate have no role in cold-acclimation of the short-tailed field vole (Microtus-agrestis). Physiol Zool 67:1117–1139Google Scholar
  38. McNab BK (1969) The economics of temperature regulation in neotropical bats. Comp Biochem Physiol A 31:227–268CrossRefGoogle Scholar
  39. McNab BK (1979) Climatic adaptation in the energetics of heteromyid rodents. Comp Biochem Physiol A 62:813–820CrossRefGoogle Scholar
  40. Mittermeier RA, Konstant WR, Hawkins AFA, Louis EE, Langrand O, Ratsimbazafy HJ, Rasoloarison RM, Ganzhorn JU, Rajaobelina S, Tattersall I, Meyers D (2006) Lemurs of Madagascar. Conservation International, Washington, DCGoogle Scholar
  41. Nagy KA (1983) Doubly-labelled water: a guide to its use. UCLA Publications, UCLA, Los Angeles, USAGoogle Scholar
  42. Nagy KA (1987) Field metabolic rate and food requirement scaling in mammals and birds. Ecol Monogr 57:111–128CrossRefGoogle Scholar
  43. Nagy KA, Bradshaw SD, Clay BT (1991) Field metabolic rate, water flux, and food requirements of short-nosed bandicoots, Isoodon obesulus (Marsupialia: Peramelidae). Aust J Zool 39:299–305CrossRefGoogle Scholar
  44. Ortmann S, Schmid J, Ganzhorn JU, Heldmaier G (1996) Body temperature and torpor in a Malagasy small primate, the mouse lemur. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold: The Tenth International Hibernation Symposium. University of New England Press, Armidale, pp 55–61Google Scholar
  45. Ortmann S, Heldmaier G, Schmid J, Ganzhorn JU (1997) Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschaften 84:28–32PubMedCrossRefGoogle Scholar
  46. Peinke DM, Brown CR (2003) Metabolism and thermoregulation in the springhare (Pedetes capensis). Comp Biochem Physiol B 173:347–353CrossRefGoogle Scholar
  47. Perret M, Aujard F, Vannier G (1998) Influence of daylength on metabolic rate and daily water loss in the male prosimian primate Microcebus murinus. Comp Biochem Physiol A 119:981–989CrossRefGoogle Scholar
  48. Radespiel U, Cepok S, Zietemann V, Zimmermann E (1998) Sex-specific usage patterns of sleeping sites in grey mouse lemurs (Microcebus murinus) in northwestern Madagascar. Am J Primatol 46:77–84PubMedCrossRefGoogle Scholar
  49. Radespiel U, Ehresmann P, Zimmermann E (2003) Species-specific usage of sleeping sites in two sympatric mouse lemur spcecies (Microcebus murinus and M. ravelobensis) in northwestern Madagascar. Am J Primatol 59:139–151PubMedCrossRefGoogle Scholar
  50. Ramanamanjato J-B, Ganzhorn JU (2001) Effects of forest fragmentation, introduced Rattus rattus and the role of exotic tree plantations and secondary vegetation for the conservation of an endemic rodent and a small lemur in littoral forests of southeastern Madagascar. Anim Conserv 4:175–183CrossRefGoogle Scholar
  51. Ricklefs RE, Konarzewski M, Daan S (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147:1047–1971CrossRefGoogle Scholar
  52. Scantlebury M, Shanas U, Speakman JR, Kupshtein H, Afik D, Haim A (2003) Energetics and water economy of common spiny mice Acomys cahirinus from north- and south-facing slopes of a Mediterranean valley. Funct Ecol 17:178–185CrossRefGoogle Scholar
  53. Scantlebury M, Oosthuizen MK, Speakman JR, Jackson CR, Bennett NC (2005) Seasonal energetics of the Hottentot golden mole (Ambysomus hottentottus longiceps) at high altitude (1500 m). Physiol Behav 84:739–745PubMedCrossRefGoogle Scholar
  54. Schad J, Ganzhorn JU, Sommer S (2005) Parasite burden and constitution of major histocompatibility complex in the malagasy mouse lemur, Microcebus murinus. Evolution 59(2):439–450PubMedGoogle Scholar
  55. Schmid J (1996) Oxygen consumption and torpor in mouse lemurs (Microcebus murinus and Microcebus myoxinus): preliminary results of a study in western Madagascar. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold: The Tenth Hibernation Symposium. University of New England Press, Armidale, pp 47–54Google Scholar
  56. Schmid J (1998) Tree holes used for resting by gray mouse lemurs (Microcebus murinus) in Madagascar: insulation capacities and energetic consequences. Int J Primatol 19:797–809CrossRefGoogle Scholar
  57. Schmid J (2000) Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: energetical consequences and biological significance. Oecologia 123:175–183CrossRefGoogle Scholar
  58. Schmid J (2001) Daily torpor in free-ranging gray mouse lemurs (Microcebus murinus) in Madagascar. Int J Primatol 22(no. 6):1021–1031CrossRefGoogle Scholar
  59. 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 170:633–641PubMedCrossRefGoogle Scholar
  60. Schmid J, Ganzhorn JU (2009) Optional strategies for reduced metabolism in gray mouse lemurs. Naturwissenschaften (in press)Google Scholar
  61. Schmid J, Ruf T, Heldmaier G (2000) Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar. J Comp Physiol B 170:59–68PubMedCrossRefGoogle Scholar
  62. Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment. University Press, CambridgeGoogle Scholar
  63. Song X, Körtner G, Geiser F (1997) Thermal relations of metabolic rate reduction in a hibernating marsupial. Am Physiol Soc 42:R2097–R2104Google Scholar
  64. Sorg J-P, Rohner U (1996) Climate and tree phenology of the dry deciduous forest of the Kirindy forest. In: Ganzhorn JU, Sorg J-P (eds) Ecology and economy of a tropical dry forest in Madagascar. Primate report. Erich Goltz GmbH, Germany, pp 57–80Google Scholar
  65. Speakman JR (1993) How should we calculate CO2 production in doubly labelled water studies of animals? Funct Ecol 7:746–750Google Scholar
  66. Speakman JR (1995) Estimation of precision in DLW studies using the two-point methodology. In: Speakman JR, Roberts SB (eds) Obesity research 3(Suppl. 1): recent advances in the doubly-labelled water technique, pp 31–41Google Scholar
  67. Speakman JR (1997) Doubly labelled water. Theory and practise. Chapman and Hall, LondonGoogle Scholar
  68. Speakman JR (1998) The history and theory of the doubly labeled water technique. Am J Clin Nutr 68:932S–938SPubMedGoogle Scholar
  69. Speakman JR (2000) The cost of living: field metabolic rates of small mammals. Adv Ecol Res 30:177–297CrossRefGoogle Scholar
  70. Speakman JR, Krol E (2005) Validation of the doubly-labelled water method in a small mammal. Physiol Biochem Zool 78:650–667PubMedCrossRefGoogle Scholar
  71. Speakman JR, Lemen C (1999) Doubly labelled water analyses program.
  72. Speakman JR, Racey PA (1988) Consequences of non steady-state CO2 production for accuracy of the doubly labeled water technique—the importance of recapture interval. Comp Biochem Physiol A 90:337–340CrossRefGoogle Scholar
  73. Speakman JR, Nagy KA, Masman D, Mook WG, Poppitt SD, Strathearn GE, Racey PA (1990) Interlaboratory comparison of different analytical techniques for the determination of O-18 abundance. Anal Chem 62:703–708CrossRefGoogle Scholar
  74. Speakman JR, Racey PA, Haim A, Webb PI, Ellison GTH, Skinner JD (1994) Interindividual and intraindividual variation in daily energy-expenditure of the pouched mouse (Saccostomus campestris). Funct Ecol 8:336–342CrossRefGoogle Scholar
  75. Thomas DW, Cloutier D (1992) Evaporative water loss by hibernating little brown bats, Myotis lucifugus. Physiol Zool 65:443–456Google Scholar
  76. Van Trigt R, Kerstel ERT, Neubert REM, Meijer HAJ, McLean M, Visser GH (2002) Validation of the DLW method in Japanese quail at different water fluxes using laser and IRMS. J Appl Physiol 93:2147–2154PubMedGoogle Scholar
  77. Vincelette M, Dumouchel J, Giroux J, Heriarivo R (2007) The Tolagnaro (Fort Dauphin) region: a brief overview of the geology, hydrology, and climatology. In: Alonso A (eds) Biodiversity, ecology and conservation of littoral ecosystems in southeastern Madagascar, Tolagnaro (Fort Dauphin). SI/MAB Series #11, Washington, DC, pp 9–18Google Scholar
  78. Visser GH, Schekkerman H (1999) Validation of the doubly labeled water method in growing precocial birds: the importance of assumptions concerning evaporative water loss. Physiol Biochem Zool 72:740–750PubMedCrossRefGoogle Scholar
  79. Wang LCH (1989) Ecological, physiological, and biochemical aspects of torpor in mammals and birds. In: Wang LCH (ed) Advances in comparative and environmental physiology. Springer, Berlin, pp 361–393Google Scholar
  80. Ward S, Scantlebury M, Krol E, Thomson PJ, Sparling C, Speakman JR (2000) Preparation of hydrogen from water by reduction with lithium aluminium hydride for the analysis of delta H-2 by isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 14:450–453PubMedCrossRefGoogle Scholar
  81. Warnecke L, Turner JM, Geiser F (2008) Torpor and basking in a small arid zone marsupial. Naturwissenschaften 95:73–78PubMedCrossRefGoogle Scholar
  82. Warren RD, Crompton RH (1998) Diet, body size and the energy costs of locomotion in saltatory primates. Folia Primatol 69(Supplement 1):86–108CrossRefGoogle Scholar
  83. Westman W, Geiser F (2004) The effect of metabolic fuel availability on thermoregulation and torpor in a marsupial hibernator. J Comp Physiol B 174:49–57PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of Experimental EcologyUniversity of UlmUlmGermany
  2. 2.Department of Animal Ecology and ConservationUniversity of HamburgHamburgGermany
  3. 3.Aberdeen Centre for Energy Regulation and Obesity (ACERO), Institute of Biological and Environmental ScienceUniversity of AberdeenAberdeenUK

Personalised recommendations