Skip to main content
SpringerLink
Log in

Hibernation and non-shivering thermogenesis in the Hottentot golden mole (Amblysomus hottentottus longiceps)

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Although heterothermy (hibernation and torpor) is a common feature among mammals, there is debate over whether it is a derived or ancestral trait relative to endothermic homeothermy. Determination of the physiological characteristics of primitive mammals is central to understanding the evolution of endothermy. Moreover, evaluation of physiological mechanisms responsible for endothermic heat production [e.g. non-shivering thermogenesis (NST)] is key to understanding how early mammals responded to historical climate changes and colonised different geographical regions. Here we investigated the capacity for NST and heterothermy in the Hottentot golden mole, a basal eutherian mammal. NST was measured as the metabolic response to injections of noradrenalin and heterothermy by recording body temperature in free-ranging animals. We found that hibernation and torpor occurred and that the seasonal phenotypic adjustment of NST capacity was similar to that found in other placental mammals. Using phylogenetically independent contrasts, we compared measured values of NST with those obtained from the literature. This showed that all variation in NST was accounted for by differences in phylogeny and not zoogeography. These findings lend support to the observation that NST and heterothermy occur in the Afrotheria, the basal placental mammalian clade. Furthermore, this work suggests that heterothermy, rather than homeothermy is a plesiomorphic trait in mammals and supports the notion that NST mechanisms are phylogenetically ancient.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adkins RM, Gelke EL, Rowe D, Honeycutt RL (2001) Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes. Mol Biol Evol 18:777–791

    PubMed  CAS  Google Scholar 

  • Augee ML, Gooden BA (1992) Monotreme hibernation—some afterthoughts. In: Augee ML (ed) Platypus and Echidnas. Royal Zoological Society of New South Wales, Sydney, pp 174–176

    Google Scholar 

  • Barnes B (1989) Freeze avoidance in a mammal: body temperatures below 0°C in an Arctic hibernator. Science 244:1593–1595

    Article  PubMed  CAS  Google Scholar 

  • Beck RMD, Bininda-Emonds ORP, Cardillo M, Liu FGR, Purvis A (2006) A higher-level MRP supertree of placental mammals. BMC Evol Biol 6:93

    Article  PubMed  CAS  Google Scholar 

  • Bennett NC, Jarvis JUM, Davis KC (1988) Daily and seasonal temperatures in the burrows of African rodent moles. S Afr J Zool 23(3):189–195

    Google Scholar 

  • Cannon B, Golozoubova V, Matthias A, Ohlsson KE, Jacobsson A, Nedergaard J (2000) Is there a life in the cold without UCP1? Uncoupling proteins and thermoregulatory thermogenesis. In: Heldmaier G, Klingenspor M (eds) Life in the cold. Springer, Berlin, pp 387–400

    Google Scholar 

  • Cannon B, Nedergaard J (2004) Brown adipose tissue: function andphysiological significance. Physiol Rev 84:277–359

    Article  PubMed  CAS  Google Scholar 

  • Chaline J, Graf J-D (1988) Phylogeny of the Arvicolidae (Rodentia): biochemical and paleontological evidence. J Mamm 69:22–33

    Article  Google Scholar 

  • Depocas F, Hart JS (1957) Use of the Pauling oxygen analyzer for measurement of oxygen consumption of animals in open-circuit systems and in a short-lag closed-circuit apparatus. J Appl Physiol 10:388–392

    PubMed  CAS  Google Scholar 

  • Dulloo AG, Samec S (2001) Uncoupling proteins: their roles in adaptive thermogenesis and substrate metabolism reconsidered. Br J Nut 86:123–139

    Article  CAS  Google Scholar 

  • Fielden LJ, Waggoner JP, Perrin MR, Hickmann GC (1990) Thermoregulation in the Namib Desert Golden Mole, Eremitalpa granti namibensis (Chrysochloridae). J Arid Environ 18:221–237

    Google Scholar 

  • Garland T, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292

    Article  Google Scholar 

  • Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Article  Google Scholar 

  • Geiser F, Baudinette RV (1990) The relationship between body mass and rate of rewarming from hibernation and daily torpor in mammals. J Exp Biol 151:349–359

    PubMed  CAS  Google Scholar 

  • Geiser F, Goodship N, Pavey CR (2002) Was basking important in the evolution of mammalian endothermy? Naturwissenschaften 89:412–414

    Article  PubMed  CAS  Google Scholar 

  • Grigg GC (2004) An evolutionary framework for studies of hibernation and short term torpor. In: Barnes M, Carey HV (eds) Life in the cold: evolution, adaptation, mechanisms, and applications. Twelth International Hibernation Symposium. Biological Papers of the University of Alaska 27. University of Alaska, Fairbanks, pp 1–11

    Google Scholar 

  • Grigg GC, Beard LA (2000) Hibernation by echidnas in mild climates: hints about the evolution of endothermy? In: Heldmaier G, Klingenspor M (eds) Life in the cold. Springer, Berlin, pp 5–20

    Google Scholar 

  • Grigg GC, Beard LA, Augee ML (2004) The evolution of endothermy and its diversity in mammals and birds. Physiol Biochem Zool 77:982–997

    Article  PubMed  Google Scholar 

  • Hayes JP, Garland T Jr (1995) The evolution of endothermy: testing the aerobic capacity model. Evolution 49:836–848

    Article  Google Scholar 

  • Heldmaier G (1971) Zitterfreie Wärmebildung und Körpergröβe bei Säugetieren. Z vergl Physiologie 73:222–248

    Article  Google Scholar 

  • Heldmaier G, Böckler H, Buchberger A, Lynch GR, Puchalski W, Steinlechner S, Wiesinger H (1985) Seasonal acclimation and thermogenesis. In: Gilles R (ed) Circulation, respiration, and metabolism. Springer, Heidelberg, pp 490–501

    Google Scholar 

  • Heldmaier G, Boeckler H, Buchberger A, Klaus S, Puchalski W, Steinlechner S, Wiesinger H (1986) Seasonal variation of thermogenesis. In: Heller HC (ed) Living in the cold: physiological and biochemical adaptations. Elsevier, New York, pp 361–372

    Google Scholar 

  • Haim A, Izhaki I (1993) The ecological significance of metabolic rate and nonshivering thermogenesis in rodents. J Therm Biol 18:71–81

    Article  Google Scholar 

  • Hickman GC (1979) A live trap and trapping technique for fossorial mammals. S Afr Zool 14:9–12

    Google Scholar 

  • Hill RW (1972) Determination of oxygen consumption by use of the paramagnetic oxygen analyzer. J Appl Physiol 33(2):261–263

    PubMed  CAS  Google Scholar 

  • Holloway JC, Geiser F (2001) Seasonal changes in the thermoenergetics of the marsupial sugar glider, Petaurus breviceps. J Comp Physiol B 171:643–650

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Jastroch M, Wuertz S, Kloas W, Klingenspor M (2005) Uncoupling protein 1 in fish uncovers an ancient evolutionary history of mammalian nonshivering thermogenesis. Physiol Genom 22:150–156

    Article  CAS  Google Scholar 

  • Klingenspor M, Helwig M, Fromme T, Brand MD, Kloas W, Taudien S, Platzer M, Jastroch M (2006) Uncoupling protein 1 is expressed in the brain of ectothermic vertebrates. Biochim Biophys Acta-Bioenerg 375–376

  • Körtner G, Geiser F (1998) Ecology of natural hibernation in the marsupial mountain pygmy-possum (Burramys parvus). Oecol 113:170–178

    Article  Google Scholar 

  • Kronfeld-Schor N, Haim A, Dayan T, Zisapel N, Heldmaier G (2000) Seasonal thermogenic acclimation of diurnally and nocturnally active desert spiny mice. Physiol Biochem Zool 73:37–44

    Article  PubMed  CAS  Google Scholar 

  • Kuyper MA (1979) A biological study of the golden mole Amblysomus hottentotus. MSc Dissertation, University of Natal, Durban

  • Lovegrove BG (1989) The cost of burrowing by the social mole rats (Bathyergidae) Cryptomys damarensis and Heterocephalus glaber: the role of soil moisture. Physiol Zool 62:449–469

    Google Scholar 

  • Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156:201–219

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Lovegrove BG (2005) Seasonal thermoregulatory responses in mammals. J Comp Physiol B 175:231–247

    Article  PubMed  Google Scholar 

  • Lovegrove BG, Génin F (2008) Torpor and hibernation in a basal placental mammal, the lesser hedgehog tenrec Echinops telfari. J Compar Physiol B (in press)

  • Lovegrove BG, Knight-Eloff A (1988) Soil and burrow temperatures, and the resource characteristics of the social mole-rat Cryptomys damarensis (Bathyergidae) in the Kalahari Desert. J Zool Lond 216:403–416

    Google Scholar 

  • Lovegrove BG, Lawes MJ, Roxburgh L (1999) Confirmation of pleisiomorphic daily torpor in mammals: the round-eared elephant shrew Maroscelides proboscideus (Macroscelidea). J Comp Physiol B 169:453–460

    Article  PubMed  CAS  Google Scholar 

  • Lovegrove BG, Raman J, Perrin MR (2001) Heterothermy in elephant shrews, Elephantulus spp. (Macroscelidea): daily torpor or hibernation? J Comp Physiol B 171:1–10

    Article  PubMed  CAS  Google Scholar 

  • Lyman CP, Blinks DC (1959) The effect of temperature on the isolated hearts of closely related hibernators and non-hibernators. J Cell Comp Physiol 54:53–63

    Article  PubMed  CAS  Google Scholar 

  • Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic Press, New York

    Google Scholar 

  • McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses. Condor 104:705–724

    Article  Google Scholar 

  • McNab BK (1978) The evolution of endothermy in the phylogeny of mammals. Am Nat 112:1–21

    Article  Google Scholar 

  • McNab BK (1992) The comparative energetics of rigid endothermy: the Arvicolidae. J Zool Lond 227:585–606

    Article  Google Scholar 

  • Malan A (1996) The origins of hibernation: a reappraisal. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold, tenth international hibernation symposium. University of New England Press, Armidale, pp 1–6

    Google Scholar 

  • Mezhzherin VA (1964) Dehnel’s phenomenon and its possible explanation. Acta Theriol 8:95–114 In Russian with English summary

    Google Scholar 

  • Michaux J, Catzeflis F (2000) The bushlike radiation of muroid rodents is exemplified by the molecular phylogeny of the LCAT nuclear gene. Mol Phylogenet Evol 17:280–293

    Article  PubMed  CAS  Google Scholar 

  • Mzilikazi N, Lovegrove BG (2002) Exogenous passive heating during arousal in free-ranging rock elephant shrews, Elephantulus myurus. Oecol 133:307–314

    Article  Google Scholar 

  • Mzilikazi N, Lovegrove BG (2004) Daily torpor in free-ranging rock elephant shrews, Elephantulus myurus: a year-long study. Physiol Biochem Zool 77:285–296

    Article  PubMed  Google Scholar 

  • Mzilikazi N, Lovegrove BG (2006) Noradrenalin induces thermogenesis in a phylogenetically ancient eutherian mammal, the rock elephant shrew, Elephantulus myurus. J Comp Physiol B 176:75–84

    Article  PubMed  CAS  Google Scholar 

  • Nedergaard J, Cannon B (1986) Brown adipose-tissue thermogenesis in neonatal and cold-adapted animals. Biochem Soc Trans 14:233–236

    PubMed  Google Scholar 

  • Pagel M (1992) A method for the analysis of comparative data. J Theor Biol 156:431–442

    Article  Google Scholar 

  • Poppitt SD, Speakman JR, Racey PA (1994) Energetics of reproduction in the Lesser Hedgehog Tenrec, Echinops telfairi (Martin). Physiol Zool 67:976–994

    Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Rose RW, West AK, Ye JM, McCormack GH, Colquhoun EQ (1999) Nonshivering thermogenesis in a marsupial (The Tasmanian bettong Bettongia gaimardi) is not attributable to brown adipose tissue. Physiol Biochem Zool 72:699–704

    Article  PubMed  CAS  Google Scholar 

  • Ruben JA (1995) The evolution of endothermy in mammals and birds: from physiology to fossils. Annu Rev Physiol 57:69–95

    Article  PubMed  CAS  Google Scholar 

  • Scantlebury M, Oosthuizen MK, Speakman JR, Jackson CR, Bennett NC (2005) Seasonal energetics of the Hottentot golden mole at 1,500 m altitude. Physiol Behav 84:739–745

    Article  PubMed  CAS  Google Scholar 

  • Scholl P (1974) Temperatureregulation beim madagassischen Igeltanrek Echinops telfairi (Martin 1838). J Comp Physiol 89:175–195

    Article  Google Scholar 

  • Skinner JD, Chimimba CT (2005) Mammals of the Southern African Sub-region. Cambridge University Press, Cambridge

    Google Scholar 

  • Steppan SJ, Adkins RM, Anderson J (2004) Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol 53:533–553

    Article  PubMed  Google Scholar 

  • Superina M, Boily P (2007) Hibernation and daily torpor in an armadillo, the pichi (Zaedyus pichiy). Comp Biochem Physiol A 148:893–898

    Article  CAS  Google Scholar 

  • Vleck D (1979) The energy cost of burrowing by the pocket gopher Thomomys bottae. Physiol Zool 52:122–125

    Google Scholar 

  • Wang LCH (1989) Ecological, physiological and biochemical aspects of torpor in mammals and birds. In: Wang LCH (ed) Advances in comparative and environmental physiology, vol 4. Springer, Heidelberg, pp 361–401

    Google Scholar 

  • Wildman DE, Uddin M, Opazo JC, Liu G, Lefort V, Guindon S, Gascuel O, Grossman LI, Romero R, Goodman M (2007) Genomics, biogeography, and the diversification of placental mammals. Proc Nat Acad Sci 104:14395–14400

    Article  PubMed  CAS  Google Scholar 

  • Wunder BA, Gettinger RD (1996) Effects of body mass and temperature acclimation on the nonshivering thermogenic response of small mammals. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adapatations to the cold: tenth international hibernation symposium. University of New England Press, Armidale, pp 1–404

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis. Prentice-Hall, New Jersey

    Google Scholar 

Download references

Acknowledgments

We would like to thank Hermien Viljoen, Low de Vries, Johnny Wilson, Nicole Hagenah, Ingrid Mathissen and Laars Erik Andersen for assistance in the field. We thank the University of Pretoria for funding for fieldwork logistics. BGL provided the anaesthetics. The work was supported in part by postdoctoral fellowships of the University of Pretoria to MS and HL and by research grants from the National Research Foundation (RSA) to NCB and BGL. BGL was also supported by a core-rolling grant and incentive grants from the University of KwaZulu-Natal Research Office; NCB was additionally supported by funds from the University of Pretoria. The experiments reported in this study comply with the current laws of the country in which the experiments were performed.

Author information

Authors and Affiliations

  1. Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Pretoria, 0002, South Africa

    M. Scantlebury, C. R. Jackson, N. C. Bennett & H. Lutermann

  2. Quercus, School of Biological Sciences, Queen’s University Belfast, Belfast, BT9 7BL, UK

    M. Scantlebury

  3. School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag, X01, Scottsville, 3209, South Africa

    B. G. Lovegrove

Authors
  1. M. Scantlebury
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. G. Lovegrove
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. R. Jackson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. C. Bennett
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. H. Lutermann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Scantlebury.

Additional information

Communicated by G. Heldmaier.

Electronic supplementary material

Below is the link to the electronic supplementary material.

360_2008_277_MOESM1_ESM.xls

360_2008_277_Fig8_ESM.jpg

360_2008_277_MOESM3_ESM.doc

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scantlebury, M., Lovegrove, B.G., Jackson, C.R. et al. Hibernation and non-shivering thermogenesis in the Hottentot golden mole (Amblysomus hottentottus longiceps). J Comp Physiol B 178, 887–897 (2008). https://doi.org/10.1007/s00360-008-0277-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-008-0277-5

Keywords

Search

Navigation