Late-born intermittently fasted juvenile garden dormice use torpor to grow and fatten prior to hibernation: Consequences for ageing processes

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1797, 2014, Pages

  Giroud, Sylvain ^a   Zahn, Sandrine ^b,c   Criscuolo, FrançOis ^b,c   Chery, Isabelle ^b,c   Blanc, StéPhane ^b,c   Turbill, Christopher ^d   Ruf, Thomas ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c CNRS   (France)

^d WESTERN SYDNEY UNIVERSITY   (Australia)

Author keywords

Doubly labelled water; Eliomys quercinus; Intermittent fasting; Pre hibernation fattening; Telomere length; Winter survival

Indexed keywords

AGING; ANIMAL; BODY COMPOSITION; DORMOUSE; EATING; FEMALE; FOOD DEPRIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIBERNATION; MALE; MOLECULAR GENETICS; PHYSIOLOGY; SEASON; TELOMERE HOMEOSTASIS; TIME FACTOR; TORPOR;

AGING; ANIMALS; BODY COMPOSITION; EATING; FEMALE; FOOD DEPRIVATION; HIBERNATION; MALE; MOLECULAR SEQUENCE DATA; MYOXIDAE; SEASONS; TELOMERE HOMEOSTASIS; TIME FACTORS; TORPOR;

EID: 84908667008     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.1131     Document Type: Article

References (56)

1. 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.
2. Heldmaier G, Ruf T. 1992 Body temperature and metabolic rate during natural hypothermia in endotherms. J. Comp. Physiol. B 162, 696–706. (doi:10.1007/BF00301619)
3. Dark J. 2005 Annual lipid cycles in hibernators: integration of physiology and behavior. Annu. Rev. Nutr. 25, 469–497. (doi:10.1146/annurev.nutr.25.050304.092514)
4. Arnold W. 1990 The evolution of marmot sociality. I. Why disperse late? Behav. Ecol. Sociobiol. 27, 229–237. (doi:10.1007/BF00164894)
5. Pilastro A, Gomiero T, Marin G. 1994 Factors affecting body mass of young fat dormice (Glis glis) at weaning and by hibernation. J. Zool. 234, 13–23. (doi:10.1111/j.1469-7998.1994.tb06053.x)
6. Geiser F, Brigham RM. 2012 The other functions of torpor. In Living in a seasonal world thermoregulatory and metabolic adaptations (eds T Ruf, C Bieber, W Arnold, E Millesi), pp. 109–121. Berlin, Germany: Springer.
7. Geiser F. 2008 Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comp. Biochem. Physiol. A 150, 176–180. (doi:10.1016/j.cbpa.2007.02.041)
8. Giroud S, Turbill C, Ruf T. 2012 Torpor use and body mass gain during pre-hibernation in late-born juvenile garden dormice exposed to food shortage. In Living in a seasonal world thermoregulatory and metabolic adaptations (eds T Ruf, C Bieber, W Arnold, E Millesi), pp. 481–491. Berlin, Germany: Springer.
9. Turbill C, Bieber C, Ruf T. 2011 Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc. R. Soc. B 278, 3355–3363. (doi:10.1098/rspb.2011.0190)
10. Turbill C, Smith S, Deimel C, Ruf T. 2012 Daily torpor is associated with telomere length change over winter in Djungarian hamsters. Biol. Lett. 8, 304–307. (doi:10.1098/rsbl.2011.0758)
11. von Zglinicki T. 2002 Oxidative stress shortens telomeres. Trends Biochem. Sci. 27, 339–344. (doi:10.1016/S0968-0004(02)02110-2)
12. Turbill C, Ruf T, Smith S, Bieber C. 2013 Seasonal variation in telomere length of a hibernating rodent. Biol. Lett. 9, 20121095. (doi:10.1098/rsbl.2012.1095)
13. Metcalfe NB, Monaghan P. 2003 Growth versus lifespan: perspectives from evolutionary ecology. Exp. Gerontol. 38, 935–940. (doi:10.1016/S0531-5565(03)00159-1)
14. Bieber C, Jusˇkaitis R, Turbill C, Ruf T. 2012 High survival during hibernation affects onset and timing of reproduction. Oecologia 169, 155–166. (doi:10.1007/s00442-011-2194-7)
15. Bieber C, Ruf T. 2004 Seasonal timing of reproduction and hibernation in the edible dormouse (Glis glis). In Life in the cold V: evolution, mechanism, adaptation, and application twelfth international hibernation symposium (eds BM Barnes, HV Carey), pp. 113–125. Fairbanks, AK: Institute of Arctic Biology, University of Alaska.
16. Kunz TH. 1974 Feeding ecology of a temperate insectivorous bat (Myotis velifer). Ecology 55, 693–711. (doi:10.2307/1934408)
17. Southwood TRE, Wint GRW, Kennedy CEJ, Greenwood SR. 2004 Seasonality, abundance, species richness and specificity of the phytophagous guild of insects on oak (Quercus) canopies. Eur. J. Entomol. 101, 43–50. (doi:10.14411/eje.2004.011)
18. Mrosovsky N, Lang K. 1980 Body weights of garden dormice, Eliomys quercinus, kept in constant conditions for two years. Comp. Biochem. Physiol. A 67, 667–669. (doi:10.1016/0300-9629(80)90257-1)
19. Bertolino S, Viano C, Currado I. 2001 Population dynamics, breeding patterns and spatial use of the garden dormouse (Eliomys quercinus) in an Alpine habitat. J. Zool. 253, 513–521. (doi:10.1017/S0952836901000474)
20. Moreno S. 1988 Reproduction of garden dormouse Eliomys quercinus lusitanicus, in southwest Spain. Mammalia 52, 401–408. (doi:10.1515/mamm-1988-0310)
21. Buchholz AC, Schoeller DA. 2004 Is a calorie a calorie? Am. J. Clin. Nutr. 79, 899S–906S.
22. 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)
23. Blanc S, Géloën A, Pachiaudi C, Gharib C, Normand S. 2000 Validation of the doubly labeled water method in rats during isolation and simulated weightlessness. Am. J. Physiol. Reg. Int. Comp. Physiol. 279, R1964–R1979.
24. Soxhlet FV. 1879 Die gewichtsanalytische Bestimmung des Milchfettes. Polytechn. J. 232, 461–465.
25. Callicott RJ, Womack JE. 2006 Real-time PCR assay for measurement of mouse telomeres. Comp. Med. 56, 17–22. See http://www.ingentaconnect.com/content/aalas/cm/2006/00000056/00000001/art00003.
26. Cawthon RM. 2002 Telomere measurement by quantitative PCR. Nucleic Acids Res. 30, E47. (doi:10.1093/nar/30.10.e47)
27. R Development Core Team. 2009 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
28. Fox J, Weisberg S. 2011 An R companion to applied regression, 22, 449 p., 2nd edn. Thousand Oaks, CA: Sage.
29. Legendre P, Legendre L. 1998 Numerical ecology: second English edition, 870 p. Amsterdam, The Netherlands: Elsevier. Developments in environmental modelling, 20.
30. Sokal RR, Rohlf FJ. 1995 Biometry. The principles and practice of statistics in biological research, 887 p, 3rd edn. New York, NY: WH. Freeman.
31. Speakman JR, Rowland A. 1999 Preparing for inactivity: how insectivorous bats deposit a fat store for hibernation. Proc. Nutr. Soc. 58, 123–131. (doi:10.1079/Pns19990017)
32. Hiebert SM. 1991 Seasonal differences in the response of rufous hummingbirds to food restriction: body mass and the use of torpor. Condor 93, 526–537. (doi:10.2307/1368184)
33. Humphries MM, Thomas DW, Kramer DL. 2001 Torpor and digestion in food-storing hibernators. Physiol. Biochem. Zool. 74, 283–292. (doi:10.1086/319659)
34. Clauss M, Streich WJ, Schwarm A, Ortmann S, Hummel J. 2007 The relationship of food intake and ingesta passage predicts feeding ecology in two different megaherbivore groups. Oikos 116, 209–216. (doi:10.1111/j.2006.0030-1299.15461.x,)
35. Bae H, Larkin JE, Zucker I. 2003 Juvenile siberian hamsters display torpor and modified locomotor activity and body temperature rhythms in response ro reduced food availability. Physiol. Biochem. Zool. 76, 858–867. (doi:10.1086/381462)
36. Overton JM, Williams TD. 2004 Behavioral and physiologic responses to caloric restriction in mice. Physiol. Behav. 81, 749–754. (doi:10.1016/j.physbeh.2004.04.025)
37. 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. (doi:10.1007/BF00571257)
38. Ortmann S, Heldmaier G. 2000 Regulation of body temperatures and energy requirements of hibernating Alpine marmots (Marmota marmota). Am. J. Physiol. Reg. Int. Comp. Physiol. 278, 698–704. See http://ajpregu.physiology.org/content/278/3/R698.
39. Ruf T, Stieglitz A, Steinlechner S, Blank JL, Heldmaier G. 1993 Cold exposure and food restriction facilitate physiological responses to short photoperiod in Djungarian hamsters (Phodopus sungorus). J. Exp. Zool. 267, 104–112. (doi:10.1002/jez.1402670203)
40. Humphries MM, Thomas DW, Kramer DL. 2003 The role of energy availability in mammalian hibernation: a cost–benefit approach. Physiol. Biochem. Zool. 76, 165–179. (doi:10.1086/367950)
41. Bieber C, Lebl K, Stalder G, Geiser F, Ruf T. 2014 Body mass dependent use of hibernation: why not prolong the active season, if they can? Funct. Ecol. 28, 167–177. (doi:10.1111/1365-2435.12173)
42. Zervanos SM, Maher CR, Waldvogel JA, Florant GL. 2010 Latitudinal differences in the hibernation characteristics of woodchucks (Marmota monax). Physiol. Biochem. Zool. 83, 135–141. (doi:10.1086/648736)
43. Giroud S 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. Reg. Int. Comp. Physiol. 297, R950–R959. (doi:10.1152/ajpregu.00214.2009)
44. Carey HV, Frank CL, Seifert JP. 2000 Hibernation induces oxidative stress and activation of NF-kB in ground squirrel intestine. J. Comp. Physiol. B 170, 551–559. (doi:10.1007/s003600000135)
45. Harlow HJ, Frank CL. 2001 The role of dietary fatty acids in the evolution of spontaneous and facultative hibernation patterns in prairie dogs. J. Comp. Physiol. B 171, 77–84. (doi:10.1007/s003600000148)
46. Wiebe WJ, Sheldon WM, Pomeroy LR. 1992 Bacterial growth in the cold: evidence for an enhanced substrate requirement. Appl. Environ. Microbiol. 58, 359–364. See http://aem.asm.org/content/58/1/359.
47. 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 Living in a seasonal world thermoregulatory and metabolic adaptations (eds T Ruf, C Bieber, W Arnold, E Millesi), pp. 231–242. Berlin, Germany: Springer.
48. Tøien Ø, Drew KL, Chao ML, Rice ME. 2001 Ascorbate dynamics and oxygen consumption during arousal from hibernation in Arctic ground squirrels. Am. J. Physiol. Reg. Int. Comp. Physiol. 281, R572–R583. See http://ajpregu.physiology.org/content/281/2/R572.
49. 2 phase of the cell cycle throughout a bout of hibernation. Comp. Biochem. Physiol. A 90, 233–236. (doi:10.1016/0300-9629(88)91109-7)
50. Vinogradova MS. 1988 Mitotic activity of stomach epithelium in the ground squirrel, Citellus erythrogenys Brandt. Comp. Biochem. Physiol. A 91, 235–239. (doi:10.1016/0300-9629(88)90410-0)
51. 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)
52. Monaghan P. 2010 Telomeres and life histories: the long and the short of it. Ann. NY Acad. Sci. 1206, 130–142. (doi:10.1111/j.1749-6632.2010.05705.x)
53. Rolfe DF, Brown GC. 1997 Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731–758. See http://physrev.physiology.org/content/77/3/731.
54. Carey HV. 1990 Seasonal changes in mucosal structure and function in ground squirrel intestine. Am. J. Physiol. Reg. Int. Comp. Physiol. 259, R385–R392. See http://ajpregu.physiology.org/content/259/2/R385.
55. Hume D, Beiglböck C, Ruf T, Frey-Roos F, Bruns U, Arnold W. 2002 Seasonal changes in morphology and function of the gastrointestinal tract of free-living alpine marmots (Marmota marmota). J. Comp. Physiol. B 172, 197–207. (doi:10.1007/s00360-001-0240-1)
56. Bieber C, Außerlechner K, Skerget C, Walzer C, Ruf T. 2011 Seasonal changes in liver size in edible dormice (Glis glis): non-invasive measurements using ultrasonography. Eur. J. Wildl. Res. 57, 657–662. (doi:10.1007/s10344-010-0476-8)