Skip to main content
Log in

The influence of natural photoperiod on seasonal torpor expression of two opportunistic marsupial hibernators

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

Abstract

Many mammals use torpor throughout the year but the individual contributions of environmental variables to seasonal changes in torpor expression are often difficult to tease apart. In many mammals, torpor is most often used opportunistically in response to decreased ambient temperature (T a ) and food availability, but information on how seasonally changing photoperiod per se influences torpor patterns is scant. Therefore, we quantified patterns of torpor use in response to natural photoperiod in captive marsupial pygmy-possums held at near-constant T a with a stable food supply over a period of 19 months. Western pygmy-possums (Cercartetus concinnus) and eastern pygmy-possums (C. nanus) used spontaneous torpor in every month of the year; in total we measured >1100 individual torpor bouts. Torpor bout duration was >60 % longer in winter than in summer and increased with decreasing day length for both species. Interestingly, the duration of torpor appeared to be adjusted at both the beginning and end of bouts because the time of entry into and rewarming from torpor relative to sunrise and sunset, respectively, changed with season. We propose that this reflects a synchronisation of torpor timing with foraging periods in the wild, which would enable animals to maintain a high body mass year-round by maximising both energy savings via torpor and energy input via food consumption. Our study suggests that photoperiod makes a significant contribution to the seasonal change in torpor bout duration of small hibernating mammals that use torpor throughout the year.

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

Access this article

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

Similar content being viewed by others

References

  • Bartoń K (2015) MuMIn: Multi-Model Inference. R package version 1.15.1. http://CRAN.R-project.org/package=MuMIn. Accessed 28 June 2016

  • Bieber C, Ruf T (2009) Summer dormancy in edible dormice (Glis glis) without energetic constraints. Naturwissenschaften 96:165–171. doi:10.1007/s00114-008-0471-z

    Article  CAS  PubMed  Google Scholar 

  • Boyer BB, Barnes BM (1999) Molecular and metabolic aspects of mammalian hibernation. Bioscience 49:713–724. doi:10.2307/1313595

    Article  Google Scholar 

  • Brown JH, Bartholomew GA (1969) Periodicity and energetics of torpor in the kangaroo mouse, Microdipodops pallidus. Ecology 70:705–709

    Article  Google Scholar 

  • Buck CL, Barnes BM (2000) Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. Am J Physiol 279:R255–R262

    CAS  Google Scholar 

  • Canguilhem B, Vaultier JP, Pévet P, Coumaros G, Masson-Pévet M, Bentz I (1977) Photoperiodic regulation of body mass, food intake, hibernation and reproduction in intact and castrated male European hamsters, Cricetus cricetus. J Comp Physiol A 163:549–557. doi:10.1007/BF00604908

    Article  Google Scholar 

  • Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181. doi:10.1152/physrev.00008.2003

    Article  CAS  PubMed  Google Scholar 

  • Carter DS, Goldman BD (1983) Antigonadal effects of timed melatonin infusion in pinealectomized male Djungarian hamsters (Phodopus sungorus sungorus): duration is the critical parameter*. Endocrinology 113:1261–1267. doi:10.1210/endo-113-4-1261

    Article  CAS  PubMed  Google Scholar 

  • Czenze Z, Willis CKR (2015) Warming up and shipping out: arousal and emergence timing in hibernating little brown bats (Myotis lucifugus). J Comp Physiol B 185:575–586. doi:10.1007/s00360-015-0900-1

    Article  PubMed  Google Scholar 

  • Dausmann KH (2014) Flexible patterns in energy savings: heterothermy in primates. J Zool 292:101–111. doi:10.1111/jzo.12104

    Article  Google Scholar 

  • Davis DE (1976) Hibernation and circannual rhythms of food consumption in marmots and ground squirrels. Q Rev Biol 51:477–514. doi:10.1086/409594

    Article  CAS  PubMed  Google Scholar 

  • French AR (1985) Allometries of the duration of torpid and euthermic intervals during mammalian hibernation: a test of the theory of metabolic control of the timing of changes in body temperature. J Comp Physiol B 156:13–19. doi:10.1007/BF00692921

    Article  CAS  PubMed  Google Scholar 

  • Geiser F (1987) Hibernation and daily torpor in two pygmy-possums (Cercartetus spp., Marsupialia). Physiol Zool 60:93–102

    Article  Google Scholar 

  • Geiser F, Baudinette RV (1987) Seasonality of torpor and thermoregulation in three dasyurid marsupials. J Comp Physiol B 157:335–344. doi:10.1007/BF00693360

    Article  Google Scholar 

  • Geiser F, Broome LS (1993) The effect of temperature on the pattern of torpor in a marsupial hibernator. J Comp Physiol B 163:133–137. doi:10.1007/BF00263598

    Article  CAS  PubMed  Google Scholar 

  • Geiser F, Heldmaier G (1995) The impact of dietary fats, photoperiod, temperature and season on morphological variables, torpor patterns, and brown adipose tissue fatty acid composition of hamsters, Phodopus sungorus. J Comp Physiol B 165:406–415. doi:10.1007/BF00387311

    Article  CAS  PubMed  Google Scholar 

  • Geiser F, Law B, Körtner G (2005) Daily torpor in relation to photoperiod in a subtropical blossom-bat, Syconycteris australis (Megachiroptera). J Therm Biol 30:574–579. doi:10.1016/j.jtherbio.2005.08.002

    Article  Google Scholar 

  • Geiser F, McAllan BM, Kenagy GJ, Hiebert SM (2007) Photoperiod affects daily torpor and tissue fatty acid composition in deer mice. Naturwissenschaften 94:319–325. doi:10.1007/s00114-006-0193-z

    Article  CAS  PubMed  Google Scholar 

  • Geiser F, Mzilikazi N (2011) Does torpor of elephant shrews differ from that of other heterothermic mammals? J Mammal 92:452–459. doi:10.1644/10-MAMM-A-097.1

    Article  Google Scholar 

  • Geiser F, Westman W, McAllan BM, Brigham RM (2006) Development of thermoregulation and torpor in a marsupial: energetic and evolutionary implications. J Comp Physiol B 176:107–116. doi:10.1007/s00360-005-0026-y

    Article  PubMed  Google Scholar 

  • Goldman BD, Darrow JM (1983) The pineal gland and mammalian photoperiodism. Nueroendocinology 37:386–396. doi:10.1159/000123579

    Article  CAS  Google Scholar 

  • Heldmaier G, Steinlechner S (1981) Seasonal pattern and energetics of short daily torpor in the Djungarian hamster, Phodopus sungorus. Oecologia 48:265–270. doi:10.1007/BF00347975

    Article  Google Scholar 

  • Hiebert S (1993) Seasonal changes in body mass and use of torpor in a migratory hummingbird. Auk 110:787–797. doi:10.2307/4088634

    Article  Google Scholar 

  • Hoelzl F, Bieber C, Cornils JS, Gerritsmann H, Stalder GL, Walzer C, Ruf T (2015) How to spend the summer? Free-living dormice (Glis glis) can hibernate for 11 months in non-reproductive years. J Comp Physiol B 185:931–939. doi:10.1007/s00360-015-0929-1

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang C, Ward SJ, Lee AK (1986) Comparison of the diets of the feathertail glider, Acrobates pygmaeus, and the eastern pygmy-possum, Cercartetus nanus (Marsupialia: Burramyidae) in sympatry. Aust Mammal 10:47–50

    Google Scholar 

  • Joy JE, Mrosovsky N (1983) Circannual cycles in golden-mantled ground squirrels: lengthening of period by low temperatures in the spring phase. J Comp Physiol A 150:233–238. doi:10.1007/BF00606373

    Article  Google Scholar 

  • Kawamichi M (1996) Ecological factors affecting annual variation in commencement of hibernation in wild chipmunks (Tamias sibiricus). J Mammal 77:731–744. doi:10.2307/1382678

    Article  Google Scholar 

  • Körtner G, Geiser F (1995) Effect of photoperiod and ambient temperature on activity patterns and body weight cycles of mountain pygmy-possums, Burramys parvus (Marsupialia). J Zool 235:311–322. doi:10.1111/j.1469-7998.1995.tb05147.x

    Article  Google Scholar 

  • Lovegrove BG (2000) Daily heterothermy in mammals: coping with unpredictable environments. In: Heldmaier G, Klingenspor M (eds) Life in the cold: eleventh international hibernation symposium. Springer-Verlag, Berlin, pp 29–40

    Chapter  Google Scholar 

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

    Google Scholar 

  • Lynch GR, White SE, Grundel R, Berger MS (1978) Effects of photoperiod, melatonin administration and thyroid block on spontaneous daily torpor and temperature regulation in the white-footed mouse, Peromyscus leucopus. J Comp Physiol B 125:157–163. doi:10.1007/BF00686752

    Article  CAS  Google Scholar 

  • McAllan BM, Dickman CR, Crowther MS (2006) Photoperiod as reproductive cue in the marsupial genus Antechinus: ecological and evolutionary consequences. Biol J Linn Soc 87:365–379. doi:10.1111/j.1095-8312.2006.00571.x

    Article  Google Scholar 

  • McKechnie AE, Mzilikazi N (2011) Heterothermy in Afrotropical mammals and birds: a review. Integr Comp Biol 51:349–363. doi:10.1093/icb/icr035

    Article  PubMed  Google Scholar 

  • Morrison PR (1964) Adaptation of small mammals to the arctic. Fed Proc 23:1202–1206

    CAS  PubMed  Google Scholar 

  • Munn AJ, Kern P, McAllan BM (2010) Coping with chaos: unpredictable food supplies intensify torpor use in an arid-zone marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). Naturwissenschaften 97:601–605. doi:10.1007/s00114-010-0670-2

    Article  CAS  PubMed  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. doi:10.1086/381470

    Article  PubMed  Google Scholar 

  • Nicol SC, Andersen NA (2002) The timing of hibernation in Tasmanian echidnas: why do they do it when they do? Comp Biochem Physiol B 131:603–611. doi:10.1016/S1096-4959(02)00018-0

    Article  PubMed  Google Scholar 

  • Park KJ, Jones G, Ransome RD (2000) Torpor, arousal and activity of hibernating greater horseshoe bats (Rhinolophus ferrumequinum). Funct Ecol 14:580–588. doi:10.1046/j.1365-2435.2000.t01-1-00460.x

    Article  Google Scholar 

  • Pengelley ET, Fisher KC (1963) The effect of temperature and photoperiod on the yearly hibernating behavior of captive golden-mantled ground squirrels (Citellus lateralis tescorum). Can J Zoolog 41:1103–1120. doi:10.1139/z63-087

  • Perret M, Aujard F (2001) Daily hypothermia and torpor in a tropical primate: synchronization by 24-h light-dark cycle. Am J Physiol-Reg I 281:1925–1933

    Google Scholar 

  • Pestell AJL (2005) Patterns of capture, genetic structure, and diet of western pygmy possums, Cercartetus concinnus Gould (Marsupialia: Burramyidae), in Innes National Park, South Australia. BAppSc (Honours) thesis, University of South Australia

  • Prendergast BJ, Nelson RJ, Zucker I (2002) Mammalian seasonal rhythms: behavior and neuroendocrine substrates. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, brain and behavior. Academic Press, San Diego, pp 93–156

    Chapter  Google Scholar 

  • R Core Team (2014). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Austria, http://www.R-project.org/

  • Rismiller PD, Heldmaier G (1987) Melatonin and photoperiod affect body temperature selection in the lizard Lacerta viridis. J Therm Biol 12:131–134. doi:10.1016/0306-4565(87)90051-9

    Article  Google Scholar 

  • Ruf T, Steinlechner S, Heldmaier G (1989) Rhythmicity of body temperature and torpor in the Djungarian hamster, Phodopus sungorus. In: Malan A, Canguilhem B (eds) Living in the Cold II. Colloque INSERM/John Libbey Eurotext, London, pp 53–61

    Google Scholar 

  • Stawski C, Geiser F (2010) Seasonality of torpor patterns and physiological variables of a free-ranging subtropical bat. J Exp Biol 213:393–399. doi:10.1242/jeb.038224

    Article  CAS  PubMed  Google Scholar 

  • Tulloch AI (2004) The importance of food and shelter for habitat use and conservation of the burramyids in Australia. In: Goldingay RL, Jackson SM (eds) The biology of Australian possums and gliders. Surrey Beatty and Sons Pty Ltd, Chipping Norton, pp 268–284

    Google Scholar 

  • Turbill C, Körtner G, Geiser F (2003) Natural use of heterothermy by a small, tree-roosting bat during summer. Physiol Biochem Zool 76:868–876. doi:10.1086/378915

    Article  PubMed  Google Scholar 

  • Turner JM, Körtner G, Warnecke L, Geiser F (2012b) Summer and winter torpor use by a free-ranging marsupial. Comp Biochem Physiol A 162:274–280. doi:10.1016/j.cbpa.2012.03.017

    Article  CAS  Google Scholar 

  • Turner JM, Warnecke L, Körtner G, Geiser F (2012a) Opportunistic hibernation by a free-ranging marsupial. J Zool 286:277–284. doi:10.1111/j.1469-7998.2011.00877.x

    Article  Google Scholar 

  • Twente JW, Twente JA (1965) Regulation of hibernating periods by temperature. P Natl Acad Sci USA 54:1058–1061

    Article  CAS  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. Springer-Verlag, Berlin, pp 361–401

    Google Scholar 

  • Warnecke L (2012) Quantifying torpor in small mammals non-invasively using infrared thermocouples. J Therm Biol 37:380–383. doi:10.1016/j.jtherbio.2012.02.002

    Article  Google Scholar 

  • Willis CKR, Goldzieher A, Geiser F (2005) A non-invasive method for quantifying patterns of torpor and activity under semi-natural conditions. J Therm Biol 30:551–556. doi:10.1016/j.jtherbio.2005.07.001

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice-Hall, New Jersey

    Google Scholar 

Download references

Acknowledgments

We thank Craig Willis for help trapping in Dorrigo. Rita Enke and Ray Dayman from the Department of the Environment provided Mallee Cliffs site access and trapping lines and Matthew Dowle assisted in the field. Nereda Christian, Daniella Rojas, Chris Wacker and Lisa Warnecke helped with colony maintenance. Lisa Warnecke also improved the manuscript with insightful comments. Julian Glos and Joachim Nopper provided statistical advice. Permits were provided by the Animal Ethics Committee of the University of New England and the New South Wales National Parks and Wildlife Service. The study was funded by grants from the Australian Research Council (FG), as well as from the University of New England and the Australian Wildlife Society (JMT).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James M. Turner.

Additional information

Communicated by I. D. Hume.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Turner, J.M., Geiser, F. The influence of natural photoperiod on seasonal torpor expression of two opportunistic marsupial hibernators. J Comp Physiol B 187, 375–383 (2017). https://doi.org/10.1007/s00360-016-1031-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-016-1031-z

Keywords

Navigation