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Photoperiod affects daily torpor and tissue fatty acid composition in deer mice

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Abstract

Photoperiod and dietary lipids both influence thermal physiology and the pattern of torpor of heterothermic mammals. The aim of the present study was to test the hypothesis that photoperiod-induced physiological changes are linked to differences in tissue fatty acid composition of deer mice, Peromyscus maniculatus (∼18-g body mass). Deer mice were acclimated for >8 weeks to one of three photoperiods (LD, light/dark): LD 8:16 (short photoperiod), LD 12:12 (equinox photoperiod), and LD 16:8 (long photoperiod). Deer mice under short and equinox photoperiods showed a greater occurrence of torpor than those under long photoperiods (71, 70, and 14%, respectively). The duration of torpor bouts was longest in deer mice under short photoperiod (9.3 ± 2.6 h), intermediate under equinox photoperiod (5.1 ± 0.3 h), and shortest under long photoperiod (3.7 ± 0.6 h). Physiological differences in torpor use were associated with significant alterations of fatty acid composition in ∼50% of the major fatty acids from leg muscle total lipids, whereas white adipose tissue fatty acid composition showed fewer changes. Our results provide the first evidence that physiological changes due to photoperiod exposure do result in changes in lipid composition in the muscle tissue of deer mice and suggest that these may play a role in survival of low body temperature and metabolic rate during torpor, thus, enhancing favourable energy balance over the course of the winter.

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Abbreviations

MUFA:

monounsaturated fatty acids

PUFA:

polyunsaturated fatty acids

SFA:

saturated fatty acids

T a :

air temperature

T b :

body temperature

UFA:

unsaturated fatty acids

\({\mathop {\text{V}}\limits^{\text{.}} }{\text{O}}_{{\text{2}}} \) :

rate of oxygen consumption

WAT:

white adipose tissue

References

  • Barnes BM, Carey HV (eds) (2004) Life in the cold: evolution, mechanisms, adaptation, and application. 12th International Hibernation Symposium. Biological Papers, University of Alaska #27. Institute of Arctic Biology, University of Alaska, Fairbanks

  • Cossins AR, Wilkinson HL (1982) The role of homeoviscous adaptation in mammalian hibernation. J Therm Biol 7:107–110

    Article  Google Scholar 

  • Dark J (2005) Annual lipid cycles in hibernators: integration of physiology and behaviour. Annu Rev Nutr 25:469–497

    Article  CAS  Google Scholar 

  • Fietz J, Tataruch F, Dausmann KH, Ganzhorn JU (2003) White adipose tissue composition in the free-ranging fat-tailed dwarf lemur (Cheirogaleus medius, Primates), a tropical hibernator. J Comp Physiol B 173:1–10

    PubMed  CAS  Google Scholar 

  • Florant GL (1998) Lipid metabolism in hibernators: the importance of essential fatty acids. Am Zool 38:331–340

    CAS  Google Scholar 

  • Frank CL (1994) Polyunsaturate content and diet selection by ground squirrels (Spermophilus lateralis). Ecology 75:458–463

    Article  Google Scholar 

  • Frank CL, Dierenfeld ES, Storey KB (1998) The relationship between lipid peroxidation, hibernation, and food selection in mammals. Am Zool 38:341–350

    CAS  Google Scholar 

  • Geiser F (1990) Influence of polyunsaturated and saturated dietary lipids on adipose tissue, brain and mitochondrial membrane fatty acid composition of a mammalian hibernator. Biochim Biophys Acta 1046:159–166

    PubMed  CAS  Google Scholar 

  • Geiser F (1991) The effect of polyunsaturated dietary lipids on the pattern of daily torpor and the fatty acid composition of tissues and membranes of the deer mouse Peromyscus maniculatus. J Comp Physiol B 161:590–597

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Geiser F, Kenagy GJ (1987) Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator. Am J Physiol 252:R897–R901

    PubMed  CAS  Google Scholar 

  • Geiser F, McAllan BM, Kenagy GJ (1994) The degree of dietary fatty acid unsaturation affects torpor patterns and lipid composition of a hibernator. J Comp Physiol B 164:299–305

    Article  PubMed  CAS  Google Scholar 

  • Hiebert SM, Fulkerson E, Lindermayer K, McClure S (2000) The effect of temperature on preference for dietary unsaturated fatty acids in the Djungarian hamster (Phodopus sungorus). Can J Zool 78:1361–1368

    Article  CAS  Google Scholar 

  • Hiebert SM, Leininger E, Huneryager R, Le L, Pannorfi R, Pike E (2003a) Dietary lipids, temperature, and melatonin: behavioural preference adjustments in hamsters consistent with the membrane homeoviscosity model. Int Comp Biol 43:1018

    Google Scholar 

  • Hiebert SM, Hauser K, Ebrahim AJ (2003b) Long day Djungarian hamsters exhibit temperature-dependent dietary fat choice. Physiol Biochem Zool 76:850–857

    Article  PubMed  Google Scholar 

  • Holloway J, Geiser F (1996) Reproductive status and torpor of the marsupial Sminthopsis crassicaudata: effect of photoperiod. J Therm Biol 21:373–380

    Article  Google Scholar 

  • Hudson JW, Scott IM (1979) Daily torpor in the laboratory mouse Mus musculus var. albino. Physiol Zool 52:205–218

    Google Scholar 

  • Hulbert AJ, Turner N, Storlien L, Else PL (2005) Dietary fats and membrane function: implications for metabolism and disease. Biol Rev 80:155–169

    Article  PubMed  CAS  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 

  • Lepage G, Roy CC (1986) Direct transesterification of all classes of lipids in a one-step reaction. J Lipid Res 27:114–120

    PubMed  CAS  Google Scholar 

  • Lovegrove BG, Raman J, Perrin MR (2001) Daily torpor in elephant shrews (Marcoscelidea: Elephantulus spp.) in response to food deprivation. J Comp Physiol B 171:11–21

    Article  PubMed  CAS  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

    Article  CAS  Google Scholar 

  • McWilliams SR, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393

    Article  Google Scholar 

  • Mitchell TW, Turner N, Hulbert AJ, Else PL, Hawley JA, Lee JS, Bruce CR, Blanksby SJ (2004) Exercise alters the profile of phospholipid molecular species in rat skeletal muscle. J Appl Physiol 97:1823–1829

    Article  PubMed  CAS  Google Scholar 

  • Munro D, Thomas DW (2004) The role of polyunsaturated fatty acids in the expression of torpor by mammals: a review. Zoology 107:29–48

    Article  PubMed  CAS  Google Scholar 

  • Olsen RE, Henderson, RJ, Ringo E (1998) The digestion and selective absorption of dietary fatty acids in Arctic charr, Salvelinus alpinus. Aquac Nutr 4:12–21

    Article  Google Scholar 

  • Opekarová M, Tanner W (2003) Specific lipid requirements of membrane proteins—a putative bottleneck in heterologous expression. Biochim Biophys Acta 1610:11–22

    Article  PubMed  Google Scholar 

  • Stamper JL, Dark J, Zucker I (1999) Photoperiod modulates torpor and food intake in Siberian hamsters challenged with metabolic inhibitors. Physiol Behav 66:113–118

    Article  PubMed  CAS  Google Scholar 

  • Steinlechner S, Heldmaier G, Weber C, Ruf T (1986) Role of photoperiod: pineal gland interaction torpor control. In: Heller HC, Musacchia XJ, Wang LCH (eds) Living in the cold. Elsevier, New York, pp 301–307

    Google Scholar 

  • Thompson GA (1992) The regulation of membrane lipid metabolism, 2nd edn. CRC, London

    Google Scholar 

  • Valencak TG, Arnold W, Tataruch F, Ruf T (2003) High content of polyunsaturated fatty acids in muscle phospholipids of a fast runner, the European brown hare (Lepus europaeus). J Comp Physiol B 173:695–702

    Article  PubMed  CAS  Google Scholar 

  • Wang LCH (1989) Ecological, physiological, and biochemical aspects of torpor in mammals and birds. In: Wang LCH (ed) Animal adaptation to cold. Springer, Berlin Heidelberg New York, pp 361–401

    Google Scholar 

  • Zhou L, Nilsson A (2001) Sources of eicosanoid precursor fatty acid pools in tissues. J Lipid Res 42:1521–1542

    PubMed  CAS  Google Scholar 

Download references

Acknowledgement

We thank Rebecca Drury for technical help. The Alexander von Humboldt Foundation and the Australian Research Council supported the work. Animal housing and experiments were conducted according to the standards of the University of Washington and National Institutes of Health (NIH) animal care guidelines.

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Authors and Affiliations

  1. Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, NSW, 2351, Australia

    Fritz Geiser, B. M. McAllan & Sara M. Hiebert

  2. Discipline of Physiology, School of Medicine (F13), University of Sydney, Sydney, NSW, 2006, Australia

    B. M. McAllan

  3. Burke Museum and Department of Biology, University of Washington, Seattle, WA, 98195, USA

    G. J. Kenagy

  4. Department of Biology, Swarthmore College, Swarthmore, PA, 19081-1390, USA

    Sara M. Hiebert

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  1. Fritz Geiser
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  2. B. M. McAllan
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  3. G. J. Kenagy
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  4. Sara M. Hiebert
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Correspondence to Fritz Geiser.

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Geiser, F., McAllan, B.M., Kenagy, G.J. et al. Photoperiod affects daily torpor and tissue fatty acid composition in deer mice. Naturwissenschaften 94, 319–325 (2007). https://doi.org/10.1007/s00114-006-0193-z

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  • DOI: https://doi.org/10.1007/s00114-006-0193-z

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