Prolonged Torpor in Goodman’s Mouse Lemur (Microcebus lehilahytsara) from the High-Altitude Forest of Tsinjoarivo, Central-Eastern Madagascar

The nocturnal mouse and dwarf lemurs from Madagascar are known to express heterothermy. Whereas dwarf lemurs (Cheirogaleus) are obligate hibernators, mouse lemurs (Microcebus) can express a great range of heterothermic responses, including daily torpor, prolonged torpor or hibernation, depending on the species, population or individual. Although there is indirect evidence of heterothermy in a handful of mouse lemur species, direct physiological confirmation is currently limited to four: Microcebus berthae(dry forest), M. ravelobensis(dry forest), M. griseorufus(spiny forest), M. murinus(dry forest/littoral forest). We studied Goodman’s mouse lemurs (M. lehilahytsara) at the high-altitude rain forest of Tsinjoarivo, central-eastern Madagascar. We captured a total of 45 mouse lemurs during pre- and post-torpor seasons. We recorded body mass and measured tail base circumference, which was used as proxy for fattening. Moreover, using telemetry, we obtained sporadic skin temperature data from a mouse lemur female between March and June. From June 9 to 16, we performed more intensive data sampling and thereby confirmed the expression of prolonged torpor in this female, when skin temperatures consistently displayed values below 25°C for more than 24 h. We documented 3 torpor bouts, 2 of which were interrupted by naturally occurring arousals. Torpor bout duration ranged from approximately 47 to maximally about 69 h. We found similarities between the Goodman’s mouse lemur torpor profile and those known from other species, including the fact that only a portion of any mouse lemur population deposits fat stores and undergoes torpor in a given year. The variable expression of heterothermy in Goodman’s mouse lemurs contrasts with obligatory hibernation displayed by two sympatric species of dwarf lemurs, suggesting cheirogaleids use a range of metabolic strategies to cope with seasonality and cold environments.

[1]  S. Reher,et al.  Variable Climates Lead to Varying Phenotypes: “Weird” Mammalian Torpor and Lessons From Non-Holarctic Species , 2020, Frontiers in Ecology and Evolution.

[2]  Hanno Gerritsmann,et al.  Dietary Lipids Affect the Onset of Hibernation in the Garden Dormouse (Eliomys quercinus): Implications for Cardiac Function , 2018, Front. Physiol..

[3]  A. Yoder,et al.  Tropical heterothermy is “cool”: The expression of daily torpor and hibernation in primates , 2018, Evolutionary anthropology.

[4]  F. Geiser,et al.  More functions of torpor and their roles in a changing world , 2017, Journal of Comparative Physiology B.

[5]  G Heldmaier,et al.  Seasonal Control of Mammalian Energy Balance: Recent Advances in the Understanding of Daily Torpor and Hibernation , 2016, Journal of neuroendocrinology.

[6]  A. Yoder,et al.  Species discovery and validation in a cryptic radiation of endangered primates: coalescent‐based species delimitation in Madagascar's mouse lemurs , 2016, Molecular ecology.

[7]  C. Cooper,et al.  Cool echidnas survive the fire , 2016, Proceedings of the Royal Society B: Biological Sciences.

[8]  C. Walzer,et al.  Hibernation in the pygmy slow loris (Nycticebus pygmaeus): multiday torpor in primates is not restricted to Madagascar , 2015, Scientific Reports.

[9]  G. Körtner,et al.  Snoozing through the storm: torpor use during a natural disaster , 2015, Scientific Reports.

[10]  G. Körtner,et al.  The importance of mammalian torpor for survival in a post-fire landscape , 2015, Biology Letters.

[11]  P. Henry,et al.  When to initiate torpor use? Food availability times the transition to winter phenotype in a tropical heterotherm , 2015, Oecologia.

[12]  B. G. Lovegrove,et al.  Mammal survival at the Cretaceous–Palaeogene boundary: metabolic homeostasis in prolonged tropical hibernation in tenrecs , 2014, Proceedings of the Royal Society B: Biological Sciences.

[13]  K. Dausmann Flexible patterns in energy savings: heterothermy in primates , 2014 .

[14]  T. Ruf,et al.  Are Tropical Small Mammals Physiologically Vulnerable to Arrhenius Effects and Climate Change?* , 2013, Physiological and Biochemical Zoology.

[15]  C Loren Buck,et al.  Metabolic Rate and Prehibernation Fattening in Free-Living Arctic Ground Squirrels , 2013, Physiological and Biochemical Zoology.

[16]  P. Henry,et al.  Individual flexibility in energy saving: body size and condition constrain torpor use , 2013 .

[17]  A. McKechnie,et al.  Heterothermy in Afrotropical mammals and birds: a review. , 2011, Integrative and comparative biology.

[18]  P. Henry,et al.  Physiological flexibility and acclimation to food shortage in a heterothermic primate , 2011, Journal of Experimental Biology.

[19]  P. Henry,et al.  Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. , 2010 .

[20]  Kathrin H. Dausmann,et al.  Torpor on Demand: Heterothermy in the Non-Lemur Primate Galago moholi , 2010, PloS one.

[21]  Kathrin H. Dausmann,et al.  Hibernation in Malagasy mouse lemurs as a strategy to counter environmental challenge , 2009, Naturwissenschaften.

[22]  J. U. Ganzhorn,et al.  Optional strategies for reduced metabolism in gray mouse lemurs , 2009, Naturwissenschaften.

[23]  B. G. Lovegrove,et al.  Torpor and hibernation in a basal placental mammal, the Lesser Hedgehog Tenrec Echinops telfairi , 2008, Journal of Comparative Physiology B.

[24]  R. Dewar,et al.  Evolution in the hypervariable environment of Madagascar , 2007, Proceedings of the National Academy of Sciences.

[25]  L. Warnecke,et al.  Torpor and basking in a small arid zone marsupial , 2007, Naturwissenschaften.

[26]  O. Schülke,et al.  Physiological ecology of cheirogaleid primates: variation in hibernation and torpor , 2007, acta ethologica.

[27]  K. Dausmann Measuring body temperature in the field—evaluation of external vs. implanted transmitters in a small mammal , 2005 .

[28]  E. Zimmermann,et al.  Seasonal changes in general activity, body mass and reproduction of two small nocturnal primates: a comparison of the golden brown mouse lemur (Microcebus ravelobensis) in Northwestern Madagascar and the brown mouse lemur (Microcebus rufus) in Eastern Madagascar , 2003, Primates.

[29]  J. Schmid Daily Torpor in Free-Ranging Gray Mouse Lemurs (Microcebus murinus) in Madagascar , 2001, International Journal of Primatology.

[30]  J. Speakman,et al.  Daily energy expenditure of the grey mouse lemur (Microcebus murinus): a small primate that uses torpor , 2000, Journal of Comparative Physiology B.

[31]  G. Heldmaier,et al.  Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar , 2000, Journal of Comparative Physiology B.

[32]  S. Atsalis Seasonal Fluctuations in Body Fat and Activity Levels in a Rain-Forest Species of Mouse Lemur, Microcebus rufus , 1999, International Journal of Primatology.

[33]  J. Schmid Tree Holes Used for Resting by Gray Mouse Lemurs (Microcebus murinus) in Madagascar: Insulation Capacities and Energetic Consequences , 1998, International Journal of Primatology.

[34]  P. Kappeler,et al.  Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus) , 1998, Behavioral Ecology and Sociobiology.

[35]  Marina B. Blanco,et al.  Evidence of prolonged torpor in Goodman’s mouse lemurs at Ankafobe forest, central Madagascar , 2016, Primates.

[36]  L. Godfrey,et al.  Hibernation Patterns of Dwarf Lemurs in the High Altitude Forest of Eastern Madagascar , 2014 .

[37]  K. Dausmann,et al.  Extreme individual flexibility of heterothermy in free-ranging Malagasy mouse lemurs (Microcebus griseorufus) , 2010, Journal of Comparative Physiology B.

[38]  G. Körtner,et al.  Hibernation and daily torpor in Australian mammals , 2010 .

[39]  M. Blanco,et al.  Reproductive Biology of Mouse and Dwarf Lemurs of Eastern Madagascar, With an Emphasis on Brown Mouse Lemurs (Microcebus rufus) at Ranomafana National Park, A Southeastern Rainforest , 2010 .

[40]  J. Schmid Torpor in the tropics: the case of the gray mouse lemur (Microcebus murinus) , 2000 .

[41]  P. Wright Lemur traits and Madagascar ecology: coping with an island environment. , 1999, American journal of physical anthropology.

[42]  G. Heldmaier,et al.  Spontaneous Daily Torpor in Malagasy Mouse Lemurs , 1997, Naturwissenschaften.