Skip to main content
Log in

Torpor in the Patagonian opossum (Lestodelphys halli): implications for the evolution of daily torpor and hibernation

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Hibernation and daily torpor are two distinct forms of torpor, and although they are related, it is not known how and in which sequence they evolved. As the pattern of torpor expressed by the oldest marsupial order the opossums (Didelphimorphia) may provide insights into the evolution of torpor, we aimed to provide the first quantitative data on the thermal biology and torpor expression of the rare Patagonian opossum (Lestodelphys halli). It is the opossum with the southernmost distribution, has a propensity of autumnal fattening, and therefore, is likely to hibernate. We captured two male Lestodelphys, which while in captivity displayed strong daily fluctuations of body temperatures (Tb) measured with implanted miniature data loggers even when they remained normothermic. In autumn and early winter, torpor was expressed occasionally when food was available, but cold exposure and food withdrawal increased torpor use. The mean Tb throughout the study was 32.2 ± 1.4 °C, the minimum Tb measured in torpid Lestodelphys was 7.7 °C, average torpor bout duration was 10.3 h, and the maximum torpor bout duration was 42.5 h. Thus, the pattern of torpor expressed by Lestodelphys was intermediate between that of daily heterotherms and hibernators suggesting that it may represent an ancestral opportunistic torpor pattern from which the derived patterns of daily torpor and seasonal hibernation diverged.

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.

Plate 1
Fig. 1
Fig. 2
Fig. 3

Abbreviations

Ta :

Ambient temperature

Tb :

Body temperature

BMR:

Basal metabolic rate

TBD:

Torpor bout duration

References

  • Barnes BM, Ritter D (1993) Patterns of body temperature change in hibernating Arctic ground squirrels. In: Carey C, Florant GL, Wunder BA, Horwitz B (eds) Life in the cold, ecological, physiological, and molecular mechanisms. Westview, Boulder, pp 119–130

    Google Scholar 

  • Batavia M, Nguyen G, Harman K, Zucker I (2013) Hibernation patterns of Turkish hamsters: influence of sex and ambient temperature. J Comp Physiol B 183:269–277

    Article  PubMed  Google Scholar 

  • Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Bozinovic F, Ruiz G, Rosenmann M (2004) Energetics and torpor of a South American “living fossil”, the microbiotheriid Dromiciops gliroides. J Comp Physiol B 174:293–297

    Article  PubMed  Google Scholar 

  • Bozinovic F, Ruiz G, Cortes A, Rosenmann M (2005) Energetics, thermoregulation and torpor in the Chilenean mouse opossum Thylamys elegans (Didelphidae). Rev Chil Hist Nat 78:199–206

    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 

  • Cooper CE, Geiser F (2008) The “minimal boundary curve for endothermy” as a predictor of heterothermy in mammals and birds: a review. J Comp Physiol B 178:1–8

    Article  PubMed  Google Scholar 

  • Cooper CE, Withers PC, Cruz-Neto AP (2009) Metabolic, ventilatory, and hygric physiology of the gracile mouse opossum (Gracilinanus agilis). Physiol Biochem Zool 82:153–162

    Article  PubMed  CAS  Google Scholar 

  • Douglas TA, Nicol SC (1993) Thermoregulation in the South American grey, short-tailed opossum (Monodelphis domestica). Proc ANZ Soc Comp Physiol Biochem 10:19

    Google Scholar 

  • Franco M, Contreras C, Cortes P, Chappell MA, Soto-Gamboa M, Nespolo RF (2012) Aerobic power, huddling and the efficiency of torpor in the South American marsupials, Dromiciops gliroides. Biol Open. doi:10.1242/bio.20122790

  • French AR (1982) Intraspecific differences in the pattern of hibernation in the ground squirrel Spermophilus beldingi. J Comp Physiol B 148:83–91

    Article  Google Scholar 

  • Geiser F (1988) Daily torpor and thermoregulation in Antechinus (Marsupialia): influence of body mass, season, development, reproduction, and sex. Oecologia 77:395–399

    Article  Google Scholar 

  • Geiser F (2008) Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comp Biochem Physiol 150:176–180

    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, Kenagy GJ (1988) Torpor duration in relation to temperature and metabolism in hibernating ground squirrels. Physiol Zool 61:442–449

    Google Scholar 

  • Geiser F, Körtner G (2010) Hibernation and daily torpor in Australian mammals. Aust Zool 35:204–215

    Article  Google Scholar 

  • Geiser F, Mzilikazi N (2011) Does torpor in elephant shrews differ from that of other heterothermic mammals? J Mammal 92:452–459

    Article  Google Scholar 

  • Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935–966

    Google Scholar 

  • Geiser F, Holloway J, Körtner G, Maddocks TA, Turbill C, Brigham RM (2000) Do patterns of torpor differ between free-ranging and captive mammals and birds? In: Heldmaier G, Klingenspor M (eds), Life in the Cold. 11th International Hibernation Symposium. Berlin Heidelberg New York: Springer. pp 95–102

  • Grant TR, Temple-Smith PD (1987) Observations on torpor the small marsupial Dromiciops australis (Marsupialia: Microbiotheriidae) from southern Chile. In Archer M (ed) Possums and Opossums. Surrey Beatty and Roy Zool Soc NSW. pp 273–277

  • Körtner G, Geiser F (2000) Torpor and activity patterns in free-ranging sugar gliders Petaurus breviceps (Marsupialia). Oecologia 123:350–357

    Article  Google Scholar 

  • Lovegrove BG (2012) A single origin of heterothermy in mammals. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world. Springer, Heidelberg, pp 3–11. doi:10.1007/978-3-642-28678-0_1

    Chapter  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Luo Z, Ji Q, Wible JR, Yuan C (2003) An early cretaceous tribosphenic mammal and metatherian evolution. Science 302:1934–1940

    Article  PubMed  CAS  Google Scholar 

  • Malan A (2010) Is the torpor-arousal cycle of hibernation controlled by a non-temperature-compensated circadian clock? J Biol Rhythm 25:166–175

    Article  Google Scholar 

  • Marshall LG (1977) Lestodelphys halli. Mamm Spec 81:1–3

    Article  Google Scholar 

  • Martin GM (2005) Intraspecific variation in Lestodelphys halli (Marsupialia: Didelphimorphia). J Mammal 86:793–802

    Article  Google Scholar 

  • Martin GM (2010) Geographic distribution and historical occurrence of Dromiciops gliroides Thomas (Marsupialia, Microbiotheria). J Mammal 91:1025–1035

    Article  Google Scholar 

  • Martin GM, Udrizar Sauthier DE (2011) Observations on the captive behavior of the rare Patagonian opossum Lestodelphys halli (Thomas, 1921) (Marsupialia, Didelphimorphia, Didelphidae). Mammalia 75:281–286

    Article  Google Scholar 

  • McKechnie AE, Mzilikazi N (2011) Heterothermy in Afrotropical mammals and birds: a review. Int Comp Biol 51:349–363

    Article  Google Scholar 

  • McNab BK (1978) The comparative energetics of neotropical marsupials. J Comp Physiol B 125:115–128

    Article  Google Scholar 

  • Morrison PR, McNab BK (1962) Daily torpor in a Brazilian murine opossum (Marmosa). Comp Biochem Physiol 6:57–68

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Nespolo RF, Verdugo C, Cortes PA, Bacigalupe LD (2010) Bioenergetics of torpor in the microbiotherid marsupial, Monito del Monte (Dromiciops gliroides): the role of temperature and food availablility. J Comp Physiol B 180:767–773

    Article  PubMed  Google Scholar 

  • O’Leary MA, Bloch JI, Flynn JJ, Gaudin TJ, Giallombardo A, Giannini NP, Goldberg SL, Kraatz BP, Luo Z, Meng J, Ni X, Novacek MJ, Perini FA, Randall ZS, Rougier GW, Sargis EJ, Silcox MT, Simmons NB, Spaulding M, Velazco PM, Weksler M, Wible JR, Cirranello AL (2013) The placental mammal ancestor and the post-K–Pg radiation of placentals. Science 339:662–667

    Article  PubMed  Google Scholar 

  • Opazo JC, Nespolo RF, Bozinovic F (1999) Arousal from torpor in the Chilean mouse-opposum (Thylamys elegans): does non-shivering thermogenesis play a role? Comp Biochem Physiol A 123:393–397

    Article  CAS  Google Scholar 

  • Pearson OP (2007) Genus Lestodelphys Tate 1934. In: Gardner AL (ed) Mammals of South America, vol 1. University of Chicago, Chicago, pp 50–51

    Google Scholar 

  • Ribiero MCP, Bicudo JEPW (2007) Oxygen consumption and thermoregulatory responses in three species of South American marsupials. Comp Biochem Physiol A 147:658–664

    Article  Google Scholar 

  • Riek A, Geiser F (2013) Heterothermy in pouched mammals—a review. J Zool: in press

  • Rojas AD, Körtner G, Geiser F (2010) Do implanted transmitters affect maximum running speed of two small marsupials? J Mammal 91:1360–1364

    Article  Google Scholar 

  • Silva-Duran IP, Bozinovic F (1999) Food availability regulates energy expenditure and torpor in the Chilean mouse-opossum Thylamys elegans. Rev Chil Hist Nat 72:371–375

    Google Scholar 

  • Twente JW, Twente JA (1965) Regulation of hibernating periods by temperature. Proc Natl Acad Sci U S A 54:1058–1061

    Article  PubMed  CAS  Google Scholar 

  • Withers PC, Cooper CE, Nespolo RF (2012) Evaporative water loss, relative water economy and evaporative partitioning of a heterothermic marsupial, the monito del monte (Dromiciops gliroides). J Exp Biol 215:2806–2813

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Gustavo Martinez for the help with anesthesia, Laureano González and Bronwyn McAllan for the help with trapping, and Mario and Susanna Martin for the accommodation and facilities. This work was supported by grants from the Australian Research Council and a Sabbatical grant from UNE to FG.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fritz Geiser.

Additional information

Communicated by: Sven Thatje

Rights and permissions

Reprints and permissions

About this article

Cite this article

Geiser, F., Martin, G.M. Torpor in the Patagonian opossum (Lestodelphys halli): implications for the evolution of daily torpor and hibernation. Naturwissenschaften 100, 975–981 (2013). https://doi.org/10.1007/s00114-013-1098-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-013-1098-2

Keywords

Navigation