Skip to main content
SpringerLink
Log in

When to initiate torpor use? Food availability times the transition to winter phenotype in a tropical heterotherm

  • Physiological ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Timing of winter phenotype expression determines individual chances of survival until the next reproductive season. Environmental cues triggering this seasonal phenotypic transition have rarely been investigated, although they play a central role in the compensation of climatic fluctuations via plastic phenotypic adjustments. Initiation of winter daily torpor use—a widespread energy-saving phenotype—could be primarily timed according to anticipatory seasonal cues (anticipatory cues hypothesis), or flexibly fine-tuned according to actual energy availability (food shortage hypothesis). We conducted a food supplementation experiment on wild heterothermic primates (grey mouse lemurs, Microcebus murinus) at the transition to the food-limited dry season, i.e. the austral winter. As expected under the food shortage hypothesis, food-supplemented individuals postponed the seasonal transition to normal torpor use by 1–2 month(s), spent four times less torpid, and exhibited minimal skin temperature 6 °C higher than control animals. This study provides the first in situ experimental evidence that food availability, rather than abiotic cues, times the launching of torpor use. Fine-tuning of the timing of seasonal phenotypic transitions according to actual food shortage should provide heterotherms with a flexible adaptive mechanism to survive unexpected environmental fluctuations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Angilletta MJ, Cooper BS, Schuler MS, Boyles JG (2010) The evolution of thermal physiology in endotherms. Front Biosci E2:861–881

    Article  Google Scholar 

  • Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc B 277:503–511

    Article  PubMed Central  PubMed  Google Scholar 

  • Bieber C, Juškaitis R, Turbill C, Ruf T (2012) High survival during hibernation affects onset and timing of reproduction. Oecologia 169:155–166

    Article  PubMed  Google Scholar 

  • Bieber C, Lebl K, Stalder G, Geiser F, Ruf T (2014) Body mass dependent use of hibernation: why not prolong the active season, if they can? Funct Ecol 28:167–177

    Article  Google Scholar 

  • Canale CI, Henry P-Y (2010) Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Clim Res 43:135–147

    Article  Google Scholar 

  • Canale CI, Perret M, Théry M, Henry P-Y (2011) Physiological flexibility and acclimation to food shortage in a heterothermic primate. J Exp Biol 214:551–560

    Article  PubMed  Google Scholar 

  • Canale CI, Perret M, Henry P-Y (2012) Torpor use during gestation and lactation in a primate. Naturwissenschaften 99:159–163

    Article  CAS  PubMed  Google Scholar 

  • Cornelius JM, Boswell T, Jenni-Eiermann S, Breuner CW, Ramenofsky M (2013) Contributions of endocrinology to the migration life history of birds. Gen Comp Endocrinol 190:47–60

    Article  CAS  PubMed  Google Scholar 

  • Dammhahn M (2012) Are personality differences in a small iteroparous mammal maintained by a life-history trade-off? Proc R Soc Lond B 279:2645–2651

    Article  Google Scholar 

  • Dammhahn M, Kappeler PM (2008a) Small-scale coexistence of two mouse lemur species (Microcebus berthae and M. murinus) within a homogeneous competitive environment. Oecologia 157:473–483

    Article  PubMed Central  PubMed  Google Scholar 

  • Dammhahn M, Kappeler PM (2008b) Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. Int J Primatol 29:1567–1589

    Article  Google Scholar 

  • Dammhahn M, Kappeler PM (2013) Seasonality and behavioral energy strategies in Microcebus berthae and M. murinus. In: Masters J, Gamba M, Génin F (eds) Leaping ahead advances in prosimian biology. Springer, New York, pp 215–223

    Google Scholar 

  • Dausmann KH (2005) Measuring body temperature in the field-evaluation of external vs. implanted transmitters in a small mammal. J Therm Biol 30:195–202

    Article  Google Scholar 

  • Dawson A (2008) Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Philos Trans R Soc Lond B 363:1621–1633

    Article  Google Scholar 

  • Dewar RE, Richard AF (2007) Evolution in the hypervariable environment of Madagascar. Proc Natl Acad Sci USA 104:13723–13727

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Doucette LI, Brigham RM, Pavey CR, Geiser F (2012) Prey availability affects daily torpor by free-ranging Australian owlet-nightjars (Aegotheles cristatus). Oecologia 169:361–372

    Article  PubMed  Google Scholar 

  • Florant GL, Healy JE (2012) The regulation of food intake in mammalian hibernators: a review. J Comp Physiol B 182:451–467

    Article  CAS  PubMed  Google Scholar 

  • Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274

    Article  CAS  PubMed  Google Scholar 

  • Geiser F (2013) Hibernation. Curr Biol 23:R188–R193

    Article  CAS  PubMed  Google Scholar 

  • Génin F, Perret M (2003) Daily hypothermia in captive grey mouse lemurs (Microcebus murinus): effects of photoperiod and food restriction. Comp Biochem Physiol B 136:71–81

    Article  PubMed  Google Scholar 

  • Gienapp P, Leimu R, Merilä J (2007) Responses to climate change in avian migration time-microevolution versus phenotypic plasticity. Clim Res 35:25–35

    Article  Google Scholar 

  • Giroud S, Blanc S, Aujard F, Bertrand F, Gilbert C, Perret M (2008) Chronic food shortage and seasonal modulations of daily torpor and locomotor activity in the grey mouse lemur (Microcebus murinus). Am J Physiol Regul Integr Comp Physiol 294:R1958–R1967

    Article  CAS  PubMed  Google Scholar 

  • Giroud S, Perret M, Gilbert C, Zahariev A, Goudable J, Le Maho Y, Oudart H, Momken I, Aujard F, Blanc S (2009) Dietary palmitate and linoleate oxidations, oxidative stress, and DNA damage differ according to season in mouse lemurs exposed to a chronic food deprivation. Am J Physiol Regul Integr Comp Physiol 297:R950–R959

    Article  CAS  PubMed  Google Scholar 

  • Giroud S, Zahn S, Criscuolo F, Chery I, Blanc S, Turbill C, Ruf T (2014) Late-born intermittently fasted juvenile garden dormice use torpor to grow and fatten prior to hibernation: consequences for ageing processes. Proc R Soc Lond B 281:20143111

    Article  Google Scholar 

  • Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Respir Physiol Neurobiol 141:317–329

    Article  PubMed  Google Scholar 

  • Helm B, Ben-Shlomo R, Sheriff MJ, Hut RA, Foster R, Barnes BM, Dominoni D (2013) Annual rhythms that underlie phenology: biological time-keeping meets environmental change. Proc R Soc Lond B 280:20130016

    Article  Google Scholar 

  • Humphries MM, Thomas DW, Kramer DL (2003a) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179

    Article  PubMed  Google Scholar 

  • Humphries MM, Kramer DL, Thomas DW (2003b) The role of energy availability in mammalian hibernation: an experimental test in free-ranging eastern chipmunks. Physiol Biochem Zool 76:180–186

    Article  PubMed  Google Scholar 

  • Kobbe S, Ganzhorn JU, Dausmann KH (2011) Extreme individual flexibility of heterothermy in free-ranging Malagasy mouse lemurs (Microcebus griseorufus). J Comp Physiol B 181:165–173

    Article  PubMed  Google Scholar 

  • Körtner G, Geiser F (2000) The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol Int 17:103–128

    Article  PubMed  Google Scholar 

  • Kraus C, Eberle M, Kappeler PM (2008) The costs of risky male behaviour: sex differences in seasonal survival in a small sexually monomorphic primate. Proc R Soc Lond B 275:1635–1644

    Article  Google Scholar 

  • Lambrechts MM, Perret P (2000) A long photoperiod overrides non-photoperiodic factors in blue tits’ timing of reproduction. Proc R Soc Lond B 267:585–588

    Article  CAS  Google Scholar 

  • Landry-Cuerrier M, Munro D, Thomas DW, Humphries MM (2008) Climate and resource determinants of fundamental and realized metabolic niches of hibernating chipmunks. Ecology 89:3306–3316

    Article  CAS  PubMed  Google Scholar 

  • Lane JE, Kruuk LEB, Charmantier A, Murie JO, Dobson FS (2012) Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 489:554–557

    Article  CAS  PubMed  Google Scholar 

  • Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc Lond B 365:3177–3186

    Article  Google Scholar 

  • Munro D, Thomas DW, Humphries MM (2005) Torpor patterns of hibernating eastern chipmunk Tamias striatus vary in response to the size and fatty acid composition of food hoards. J Anim Ecol 74:692–700

    Article  Google Scholar 

  • Ozgul A, Childs DZ, Oli MK, Armitage KB, Blumstein DT, Olson LE, Tuljapurkar S, Coulson T (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature 466:482–485

    Article  CAS  PubMed  Google Scholar 

  • Patil VP, Morrison SF, Karels TJ, Hik DS (2013) Winter weather versus group thermoregulation: what determines survival in hibernating mammals? Oecologia 173:139–149

    Article  CAS  PubMed  Google Scholar 

  • Paul MJ, Galang J, Schwartz WJ, Prendergast BJ (2009) Intermediate-duration day lengths unmask reproductive responses to nonphotic environmental cues. Am J Physiol Regul Integr Comp Physiol 296:R1613–R1619

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Perret M, Aujard F (2001) Regulation by photoperiod of seasonal changes in body mass and reproductive function in gray mouse lemurs (Microcebus murinus): differential responses by sex. Int J Primatol 22:5–24

    Article  Google Scholar 

  • Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233

    Article  Google Scholar 

  • Rasoazanabary E (2006) Male and female activity patterns in Microcebus murinus during the dry season at Kirindy forest, western Madagascar. Int J Primatol 27:437–464

    Article  Google Scholar 

  • Reed TE, Waples RS, Schindler DE, Hard JJ, Kinnison MT (2010) Phenotypic plasticity and population viability: the importance of environmental predictability. Proc R Soc Lond B 277:3391–3400

    Article  Google Scholar 

  • Schmid J (1998) Tree holes used for resting by gray mouse lemurs (Microcebus murinus) in Madagascar: insulation capacities and energetic consequences. Int J Primatol 19:797–809

    Article  Google Scholar 

  • Schmid J (2001) Daily torpor in free-ranging gray mouse lemurs (Microcebus murinus) in Madagascar. Int J Primatol 22:1021–1031

    Article  Google Scholar 

  • Schmid J, Ganzhorn JU (2009) Optional strategies for reduced metabolism in gray mouse lemurs. Naturwissenschaften 96:737–741

    Article  CAS  PubMed  Google Scholar 

  • Schmid J, Kappeler PM (1998) Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus). Behav Ecol Sociobiol 43:125–132

    Article  Google Scholar 

  • Sheriff MJ, Kenagy GJ, Richter M, Lee T, Tøien O, Kohl F, Buck CL, Barnes BM (2011) Phenological variation in annual timing of hibernation and breeding in nearby populations of arctic ground squirrels. Proc R Soc Lond B 278:2369–2375

    Article  Google Scholar 

  • Sheriff MJ, Williams CT, Kenagy GJ, Buck CL, Barnes BM (2012) Thermoregulatory changes anticipate hibernation onset by 45 days: data from free-living arctic ground squirrels. J Comp Physiol B 182:841–847

    Article  PubMed  Google Scholar 

  • Sheriff MJ, Fridinger RW, Tøien Ø, Barnes BM, Buck CL (2013a) Metabolic rate and prehibernation fattening in free-living arctic ground squirrels. Physiol Biochem Zool 86:515–527

    Article  PubMed  Google Scholar 

  • Sheriff MJ, Richter MM, Buck CL, Barnes BM (2013b) Changing seasonality and phenological responses of free-living male arctic ground squirrels: the importance of sex. Philos Trans R Soc Lond B 368:20120480

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Terrien J, Perret M, Aujard F (2010) Gender markedly modulates behavioral thermoregulation in a non-human primate species, the mouse lemur (Microcebus murinus). Physiol Behav 101:469–473

    Article  CAS  PubMed  Google Scholar 

  • Thomas DW, Blondel J, Perret P, Lambrechts MM, Speakman JR (2001) Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science 291:2598–2600

    Article  CAS  PubMed  Google Scholar 

  • Turbill C, Bieber C, Ruf T (2011) Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc R Soc Lond B 278:3355–3363

    Article  Google Scholar 

  • Visser ME, Caro SP, van Oers K, Schaper SV, Helm B (2010) Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philos Trans R Soc Lond B 365:3113–3127

    Article  CAS  Google Scholar 

  • Vuarin P, Henry P-Y (2014) Field evidence for a proximate role of food shortage in the regulation of hibernation and daily torpor: a review. J Comp Physiol B 184:683–697

    Article  PubMed  Google Scholar 

  • Vuarin P, Dammhahn M, Henry P-Y (2013) Individual flexibility in energy saving: body size and condition constrain torpor use. Funct Ecol 27:793–799

    Article  Google Scholar 

  • Williams CT, Barnes BM, Kenagy GJ, Buck CL (2014) Phenology of hibernation and reproduction in ground squirrels: integration of environmental cues with endogenous programming. J Zool 292:112–124

    Article  Google Scholar 

Download references

Acknowledgments

We acknowledge the support of this study by Prof. Daniel Rakotondravony and the other members of the Département de Biologie Animale, Université d’Antananarivo, the Commission Tripartite, and the CAFF of the Direction des Eaux et Forêts, and the CNFEREF Morondava. This study was partly funded by CNRS and MNHN (UMR 7179), the German Primate Centre and the Ethologische Gesellschaft. The authors declare that they have no conflict of interest. We thank Martine Perret, Rodin Rasoloarison and Léonard Razafimanantsoa for their support, as well as Susanne Schliehe-Diecks, Bruno Tsiverimana, Jean-Pierre Tolojanahary and the Kirindy team for assistance in the field.

Author information

Author notes

  1. Melanie Dammhahn

    Present address: Animal Ecology, Institute for Biochemistry and Biology, University of Potsdam, Maulbeerallee 1, 14469, Potsdam, Germany

Authors and Affiliations

  1. Mécanismes adaptatifs et Evolution (MECADEV UMR 7179), Sorbonne Universités, Muséum National d’Histoire Naturelle, Centre National de la Recherche Scientifique, 1 avenue du Petit Château, 91800, Brunoy, France

    Pauline Vuarin & Pierre-Yves Henry

  2. Behavioral Ecology and Sociobiology Unit, German Primate Centre, Leibniz Institute for Primate Research, Kellnerweg 4, 37077, Göttingen, Germany

    Melanie Dammhahn & Peter M. Kappeler

  3. Department of Sociobiology/Anthropology, Johann-Friedrich-Blumenbach Institute of Zoology and Anthropology, University of Göttingen, Kellnerweg 6, 37077, Göttingen, Germany

    Peter M. Kappeler

Authors
  1. Pauline Vuarin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Melanie Dammhahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter M. Kappeler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pierre-Yves Henry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pierre-Yves Henry.

Additional information

Communicated by Joanna E. Lambert.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vuarin, P., Dammhahn, M., Kappeler, P.M. et al. When to initiate torpor use? Food availability times the transition to winter phenotype in a tropical heterotherm. Oecologia 179, 43–53 (2015). https://doi.org/10.1007/s00442-015-3328-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3328-0

Keywords

Search

Navigation