A Functional Nexus between Photoperiod Acclimation, Torpor Expression and Somatic Fatty Acid Composition in a Heterothermic Mammal

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Geiser, Fritz ^a,b   Klingenspor, Martin ^a,c   McAllan, Bronwyn M ^a,b,d  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF NEW ENGLAND   (Australia)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; LIPID; SATURATED FATTY ACID; UNSATURATED FATTY ACID;

ACCLIMATIZATION; ANIMAL EXPERIMENT; ARTICLE; BODY MASS; BODY TEMPERATURE; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; FEMALE; HAMSTER; HEART MUSCLE; LEG MUSCLE; LIPID COMPOSITION; MALE; NONHUMAN; PHODOPUS SUNGORUS; PHOTOPERIODICITY; SEASONAL VARIATION;

ACCLIMATIZATION; ADIPOSE TISSUE, BROWN; ANIMALS; BODY MASS INDEX; CRICETINAE; FATTY ACIDS; MAMMALS; MUSCLES; ORGAN SIZE; PHOTOPERIOD; REPRODUCTION; SEASONS; TEMPERATURE; TORPOR;

EID: 84878094320     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063803     Document Type: Article

References (46)

1. Hickman CP, Roberts LS, Keen SL, Eisenhour DJ, Larson A, et al. (2011) Integrated Principles of Zoology. New York. McGraw-Hill.
2. Carey HV, Andrews MT, Martin SL, (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83: 1153-1181.
3. Geiser F, Turbill C, (2009) Hibernation and daily torpor minimize mammalian extinctions. Naturwissenschaften 96: 1235-1240.
4. 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 Verlag, Berlin, Heidelberg. 3-12.
5. Stawski C, Geiser F, (2012) Will temperature effects or phenotypic plasticity determine the thermal response of a heterothermic tropical bat to climate change? PLoS ONE 7 (7): e40278.
6. Boyer BB, Barnes BM, (1999) Molecular and metabolic aspects of mammalian hibernation. Bioscience 49: 713-724.
7. Steinlechner S, Heldmaier G, Weber C, Ruf T (1986) Role of photoperiod: pineal gland interaction torpor control. In: Heller HC, Musacchia XJ and Wang LCH eds. Living in the Cold. New York. Elsevier. 301-307.
8. Geiser F, Kenagy GJ, (1987) Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator. Am J Physiol 252: R897-R901.
9. Frank CL, (1994) Polyunsaturate content and diet selection by ground squirrels (Spermophilus lateralis). Ecology 75: 458-463.
10. 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.
11. Schalk G, Brigham RM, (1995) Prey selection by insectivorous bats: are essential fatty acids important? Can J Zool 73: 1855-1859.
12. Florant GL, (1998) Lipid metabolism in hibernators: the importance of essential fatty acids. Amer Zool 38: 331-340.
13. Dark J, (2005) Annual lipid cycles in hibernators: integration of physiology and behaviour. Annu Rev Nutr 25: 469-497.
14. Ruf T, Arnold W, (2008) Effects of polyunsaturated fatty acids on hibernation and torpor: a review and a hypothesis. Am J Physiol 294: R1044-R1052.
15. Hulbert AJ, Abbott SK, (2012) Nutritional ecology of essential fatty acids: an evolutionary perspective. Aust J Zool 59: 369-379.
16. Arnold W, Ruf T, Frey-Roos F, Bruns U, (2011) Diet-independent remodelling of cellular membranes precedes seasonally changing body temperature in a hibernator. PLoS ONE 6(4): e18641 Doi:10.1371/journal.pone.0018641.
17. 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.
18. Hill RW, (1975) Daily torpor in Peromyscus leucopus on an adequate diet. Comp Biochem Physiol A 51: 413-423.
19. Lynch GR, White SE, Grundel R, Berger MS, (1978) Effects of photoperid, 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.
20. Tannenbaum MG, Pivorun EB, (1989) Summer torpor in montane Peromyscus maniculatus. Am Midl Nat 121: 194-197.
21. Figala J, Hoffmann K, Goldau G, (1973) Zur Jahresperiodik beim djungarischen Zwerghamster Phodopus sungorus Pallas. Oecologia 12: 89-118.
22. Heldmaier G, Steinlechner S, (1981) Seasonal pattern and energetics of short daily torpor in the Djungarian hamster, Phodopus sungorus. Oecologia 48: 265-270.
23. Ruf T, Klingenspor M, Preis H, Heldmaier G, (1991) Daily torpor in the Djungarian hamster (Phodopus sungorus): interactions with food intake, activity, and social behaviour. J Comp Physiol B 160: 609-615.
24. Diedrich V, Steinlechner S (2012) Spontaneous daily torpor versus fasting-induced torpor in the Djungarian hamster (Phodopus sungorus): two sides of a medal or distinct phenomena? In: Ruf T, Bieber C, Arnold W, Millesi E eds. Living in a seasonal world. Berlin, Heidelberg. Springer Verlag. 231-242.
25. 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.
26. Hiebert SM, Hauser K, Ebrahim AJ, (2003) Djungarian hamsters exhibit temperature-dependent dietary fat choice in long day. Physiol Biochem Zool 76: 850-857.
27. Klingenspor M, (2003) Cold-induced recruitment of brown adipose tissue thermogenesis. Experimental Physiology 88 (1):: 141-148.
28. Jastroch M, Withers KW, Taudien S, Frappell PB, Helwig M, et al. (2008) Marsupial uncoupling protein 1 sheds light on the evolution of mammalian nonshivering thermogenesis. Physiol Genomics 32: 161-169.
29. Swoap SJ, Gutilla MJ, (2009) Cardiovascular changes during daily torpor in the laboratory mouse. Am J Physiol 297: R769-R774.
30. Klingenspor M, Klaus S, Wiesinger H, Heldmaier G, (1989) Short photoperiod and cold activate brown fat lipase in the Djungarian hamster. Am J Physiol 257: R1123-R1127.
31. Hoffmann K, (1978) Effects of short photoperiod on puberty, growth and moult in the Djungarian hamster (Phodopus sungorus). J Reprod Fert 54: 29-35.
32. Schlatt S, Niklowitz P, Hoffmann K, Nieschlag E, (1993) Influence of short photoperiod on reproductive organs and estrous cycles of normal and pinealectomized female Djungarian hamsters, Phodopus sungorus. Biol Reprod 49: 243-250.
33. Hoffman RA, (1964) Speculations on the regulation of hibernation. Mammalian Hibernation II. Ann Acad Sci Fenn A IV. Biologica 71: 199-216.
34. Barnes BM (1996) Relationship between hibernation and reproduction in male ground squirrels. In: Geiser F, Hulbert AJ and Nicol SC eds. Adaptations to the Cold: Tenth International Hibernation Symposium. Armidale. University of New England Press. 71-80.
35. Mzilikazi N, Lovegrove BG, (2002) Reproductive activity influences thermoregulation and torpor in pouched mice, Saccostomus campestris. J Comp Physiol B 172: 7-16.
36. Morrow G, Nicol SC, (2009) Cool sex? Hibernation and reproduction overlap in the echidna. PLoS ONE 4 (6): e6070 doi:10.1371/journal.pone.0006070.
37. Geiser F, Brigham RM (2012) The other functions of torpor. In: Ruf T, Bieber C, Arnold W, Millesi E eds. Living in a seasonal world. Berlin, Heidelberg. Springer Verlag. Pp 109-121.
38. McAllan BM, Feay N, Bradley AJ, Geiser F, (2012) The influence of reproductive hormones on the torpor patterns of the marsupial Sminthopsis macroura: Bet-hedging in an unpredictable environment. Gen Comp Endocrinol 179: 265-276.
39. 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.
40. Geiser F, (1991) The effect of unsaturated and saturated 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.
41. Rojas AD, Körtner G, Geiser F, (2012) Cool running: locomotor performance at low body temperature in mammals. Biol Lett 8: 868-870.
42. 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.
43. Giroud S, Perret M, Gilbert C, Zahariev A, Goudable J, et al. (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 297: R950-R959.
44. Price ER, Armstrong C, Gugliemo CG, Staples JF, (2013) Selective mobilization of saturated fatty acids in isolated adipocites of hibernating 13-lined ground squirrels Ictidomys tridecemlineatus. Physiol Biochem Zool 86: 205-212.
45. Aloia RC, Raison JK, (1989) Membrane function in mammalian hibernation. Biochim Biophys Acta 988: 123-146.
46. Phillips R, Ursell T, Wiggins P, Sens P, (2009) Emerging roles for lipids and shaping membrane-protein function. Nature 459: 379-385.