Body mass dependent use of hibernation: Why not prolong the active season, if they can?

Functional Ecology

Volumn 28, Issue 1, 2014, Pages 167-177

  Bieber, Claudia ^a,b   Lebl, Karin ^a   Stalder, Gabrielle ^a   Geiser, Fritz ^b   Ruf, Thomas ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b UNIVERSITY OF NEW ENGLAND   (Australia)

Author keywords

Body fat reserves; Edible dormouse; Hypothermia; Life history strategy; Predation

Indexed keywords

BIOENERGETICS; BODY MASS; BODY TEMPERATURE; CLIMATE CHANGE; ENVIRONMENTAL CONDITIONS; GLOBAL CLIMATE; HIBERNATION; IMMUNOCOMPETENCE; LIFE HISTORY TRAIT; PREDATION; RODENT; SEASONALITY; SURVIVAL; TORPOR;

ANIMALIA; MAMMALIA; MYOXIDAE; MYOXUS GLIS;

EID: 84892851262     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12173     Document Type: Article

References (75)

1. Akaike, H. (1973) Information theory and extension of the maximum likelihood principle. Proceedings of 2nd International Symposium on Information Theory (eds B.N. Petrov & F. Csaki), pp. 267-281. Akademia Kaido, Budapest, Hungary.
2. Arnold, W., Ruf, T., Frey-Roos, F. & Bruns, U. (2011) Diet-independent remodeling of cellular membranes precedes seasonally changing body temperature in a hibernator. PLoS ONE, 6, e18641.
3. Barton, K. (2012) MuMIn: Multi-model inference. R package version 1.7.2. http://CRAN.R-project.org/package=MuMIn.
4. Bates, D., Maechler, M. & Bolker, B. (2011) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42. http://CRAN.R-project.org/package=lme4.
5. Bieber, C. (1998) Population dynamics, sexual activity, and reproduction failure in the fat dormouse (Myoxus glis). Journal of Zoology, 244, 223-229.
6. Bieber, C. & Ruf, T. (2009a) Habitat differences affect life history tactics of a pulsed resource consumer, the edible dormouse (Glis glis). Population Ecology, 51, 481-492.
7. Bieber, C. & Ruf, T. (2009b) Summer dormancy in edible dormice (Glis glis) without energetic constraints. Naturwissenschaften, 96, 165-171.
8. Bieber, C. & Ruf, T. (2012) Does age matter? Effects of age on hibernation patterns in edible dormice (Glis glis). Living in a Seasonal World (eds T. Ruf, C. Bieber, W. Arnold & E. Millesi), pp. 133-142. Springer-Verlag, Berlin, Heidelberg.
9. 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. European Journal of Wildlife Research, 57, 657-662.
10. Bieber, C., Juškaitis, R., Turbill, C. & Ruf, T. (2012) High survival during hibernation affects onset and timing of reproduction. Oecologia, 169, 155-166.
11. Boon, A.K., Réale, D. & Boutin, S. (2008) Personality, habitat use, and their consequences for survival in North American red squirrels (Tamiasciurus hudsonicus). Oikos, 117, 1321-1328.
12. Brown, L.N. (1970) Population dynamics of the Western jumping mouse (Zapus princeps) during a four-year study. Journal of Mammalogy, 51, 651-658.
13. Brown, J.C.L., Chung, D.J., Belgrave, K.R. & Staples, J.F. (2012) Mitochondrial metabolic suppression and reactive oxygen species production in liver and skeletal muscle of hibernating thirteen-lined ground squirrels. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 302, R15-R28.
14. Bryant, A.A. & Page, R.E. (2005) Timing and causes of mortality in the endangered Vancouver Island marmot (Marmota vancouverensis). Canadian Journal of Zoology, 83, 674-682.
15. Buck, C.L. & Barnes, B.M. (1999) Annual cycle of body composition and hibernation in free-living arctic ground squirrels. Journal of Mammalogy, 80, 430-442.
16. Burnham, K.P. & Anderson, D.R. (2002) Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach, 2nd edn. Springer-Verlag, New York.
17. Burton, R.S. & Reichman, O.J. (1999) Does immune challenge affect torpor duration? Functional Ecology, 13, 232-237.
18. Buzadžić, B., Spasić, M., Saičić, Z.S., Radojičić, R., Petrović, V.M. & Halliwell, B. (1990) Antioxidant defenses in the ground squirrel Citellus citellus 2. The effect of hibernation. Free Radical Biology and Medicine, 9, 407-413.
19. Canale, C.I. & Henry, P.-Y. (2011) Energetic costs of the immune response and torpor use in a primate. Functional Ecology, 25, 557-565.
20. Carey, H.V., Frank, C.L. & Seifert, J.P. (2000) Hibernation induces oxidative stress and activation of NF-kappa B in ground squirrel intestine. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 170, 551-559.
21. Christe, P., Keller, L. & Roulin, A. (2006) The predation cost of being a male: implications for sex-specific rates of ageing. Oikos, 114, 381-384.
22. Clemens, L.E., Heldmaier, G. & Exner, C. (2009) Keep cool: memory is retained during hibernation in Alpine marmots. Physiology and Behavior, 98, 78-84.
23. Darwin, C.R., ed. (1839) Journal and Remarks, 1832-1836. Henry, Colburn, London.
24. Fietz, J. & Weis-Dootz, T. (2012) Stranded on an island: consequences of forest fragmentation for body size variations in an arboreal mammal, the edible dormouse (Glis glis). Population Ecology, 54, 313-320.
25. Fietz, J., Pflug, M., Schlund, W. & Tataruch, F. (2005) Influences of the feeding ecology on body mass and possible implications for reproduction in the edible dormouse (Glis glis). Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 175, 45-55.
26. Fisher, K.C., ed. (1964) On the mechanisms of periodic arousal in the hibernating ground squirrel Helsinki.
27. Florant, G.L. (1998) Lipid metabolism in hibernators: the importance of essential fatty acids. American Zoologist, 38, 331-340.
28. Florant, G.L., Hester, L., Ameenuddin, S. & Rintoul, D.A. (1993) The effect of a low essential fatty acid diet on hibernation in marmots. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 264, R747-R753.
29. Frank, C.L. & Storey, K.B. (1995) The optimal depot fat composition for hibernation by golden-mantled ground squirrels (Spermophilus lateralis). Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology, 164, 536-542.
30. French, A.R. (1982) Effects of temperature on the duration of arousal episodes during hibernation. Journal of Applied Physiology, 52, 216-220.
31. French, A.R. (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. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 156, 13-19.
32. French, A.R. (1990) Age-class differences in the pattern of hibernation in yellow-bellied marmots, Marmota flaviventris. Oecologia, 82, 93-96.
33. Garces, R. & Mancha, M. (1993) One-step lipid extraction and fatty acid methyl esters preparation from fresh plant tissues. Analytical Biochemistry, 211, 139-143.
34. Geiser, F. (1988) Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 158, 25-37.
35. 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. Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology, 161, 590-597.
36. Geiser, F. (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annual Review of Physiology, 66, 239-274.
37. Geiser, F. & Kenagy, G.J. (1987) Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 252, R897-R901.
38. Geiser, F. & Ruf, T. (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiological Zoology, 68, 935-966.
39. Hackländer, K. & Arnold, W. (1999) Male-caused failure of female reproduction and its adaptive value in alpine marmots (Marmota marmota). Behavioral Ecology, 10, 592-597.
40. Hall, M. (1832) On hybernation. Philosophical Transactions of the Royal Society of London, 122, 335-360.
41. Harlow, H.J. & Frank, C.L. (2001) The role of dietary fatty acids in the evolution of spontaneous and facultative hibernation patterns in prairie dogs. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 171, 77-84.
42. Heldmaier, G. & Ruf, T. (1992) Body temperature and metabolic rate during natural hypothermia in endotherms. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 162, 696-706.
43. Humphries, M.H., Kramer, D.L. & Thomas, D.W. (2003a) The role of energy availability in mammalian hibernation: an experimental test in free ranging eastern chipmunks. Physiological and Biochemical Zoology, 76, 180-186.
44. Humphries, M.M., Thomas, D.W. & Kramer, D.L. (2003b) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiological and Biochemical Zoology, 76, 165-179.
45. Karels, T.J., Byrom, A.E., Boonstra, R. & Krebs, C.J. (2000) The interactive effects of food and predators on reproduction and overwinter survival of arctic ground squirrels. Journal of Animal Ecology, 69, 235-247.
46. Kirkwood, T.B.L. (2002) Evolution of ageing. Mechanisms of Ageing and Development, 123, 737-745.
47. Lebl, K., Kürbisch, K., Bieber, C. & Ruf, T. (2010) Energy or information? The role of seed availability for reproductive decisions in edible dormice. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 180, 447-456.
48. Lebl, K., Bieber, C., Adamík, P., Fietz, J., Morris, P., Pilastro, A. et al. (2011a) Survival rates in a small hibernator, the edible dormouse: a comparison across Europe. Ecography, 34, 683-692.
49. Lebl, K., Rotter, B., Kürbisch, K., Bieber, C. & Ruf, T. (2011b) Local environmental factors affect reproductive investment in female edible dormice. Journal of Mammalogy, 92, 926-933.
50. Lima, S.L. (1998) Nonlethal effects in the ecology of predator-prey interactions. BioScience, 48, 25-34.
51. Malan, A. (2010) Is the torpor-arousal cycle of hibernation controlled by a non-temperature-compensated circadian clock? Journal of Biological Rhythms, 25, 166-175.
52. Michener, G.R. (1978) Effect of age and parity on weight gain and entry into hibernation in Richardson's ground squirrels. Canadian Journal of Zoology, 56, 2573-2577.
53. Michener, G.R. (2004) Hunting techniques and tool use by north American badgers preying on Richardson's ground squirrels. Journal of Mammalogy, 85, 1019-1027.
54. Millesi, E., Huber, S., Everts, L.G. & Dittami, J.P. (1999) Reproductive decisions in female European ground squirrels: factors affecting reproductive output and maternal investment. Ethology, 105, 163-175.
55. Millesi, E., Prossinger, H., Dittami, J.P. & Fieder, M. (2001) Hibernation effects on memory in European ground squirrels (Spermophilus citellus). Journal of Biological Rhythms, 16, 264-271.
56. Nunes, S., Muecke, E.-M. & Holekamp, K.E. (2002) Seasonal effects of food provisioning on body fat, insulin, and corticosterone in free-living juvenile Belding's ground squirrels (Spermophilus beldingi). Canadian Journal of Zoology, 80, 366-371.
57. Pilastro, A., Gomiero, T. & Marin, G. (1994) Factors affecting body mass of young fat dormice (Glis glis) at weaning and by hibernation. Journal of Zoology, 234, 13-23.
58. Pilastro, A., Tavecchia, G. & Marin, G. (2003) Long living and reproduction skipping in the fat dormouse. Ecology, 84, 1784-1792.
59. Popescu, F.D., Hackländer, K., Arnold, W. & Ruf, T. (2011) Effects of season and reproductive state on lipid intake and fatty acid composition of gastrointestinal tract contents in the European hare. Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology, 181, 681-689.
60. Pörschmann, U. & Spieth, H.R. (2011) Aestivation in Pieris brassicae (L.) affects the parasitoid load caused by Cotesia glomerata (L.). Entomological Science, 14, 31-36.
61. Prendergast, B.J., Freeman, D.A., Zucker, I. & Nelson, R.J. (2002) Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 282, R1054-R1062.
62. R Development Core Team. (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
63. Ricklefs, R.E. (2010) Insights from comparative analyses of aging in birds and mammals. Aging Cell, 9, 273-284.
64. Ruf, T. & Arnold, W. (2008) Effects of polyunsaturated fatty acids on hibernation and torpor: a review and hypothesis. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 294, R1044-R1052.
65. Ruf, T., Fietz, J., Schlund, W. & Bieber, C. (2006) High survival in poor years: life history tactics adapted to mast seeding in the edible dormouse. Ecology, 87, 372-381.
66. Schaefer, A., Piquard, F. & Haberey, P. (1976) Food self-selection during spontaneous body weight variations in the dormouse (Glis glis L.). Comparative Biochemistry and Physiology Part A: Physiology, 55, 115-118.
67. Schaub, M. & Vaterlaus-Schlegel, C. (2001) Annual and seasonal variation of survival rates in the garden dormouse (Eliomys quercinus). Journal of Zoology, 255, 89-96.
68. Schlund, W., Scharfe, F. & Ganzhorn, J.U. (2002) Long-term comparison of food availability and reproduction in the edible dormouse (Glis glis). Mammalian Biology, 67, 219-223.
69. Trombulak, S.C. (1989) Running speed and body mass in Belding's ground squirrels. Journal of Mammalogy, 70, 194-197.
70. Turbill, C., Bieber, C. & Ruf, T. (2011) Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proceedings of the Royal Society B: Biological Sciences, 278, 3355-3363.
71. Turbill, C., Smith, S., Deimel, C. & Ruf, T. (2012) Daily torpor is associated with telomere length change over winter in Djungarian hamsters. Biology Letters, 8, 304-307.
72. Turbill, C., Ruf, T., Smith, S. & Bieber, C. (2013) Seasonal variation in telomere length of a hibernating rodent. Biology Letters, 9, 20121095.
73. Valencak, T.G., 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). Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology, 173, 695-702.
74. Vietinghoff-Riesch, A.F.V. (1960) Der Siebenschläfer (ed. D. Müller-Using), pp. 1-196. Gustav Fischer Verlag, Jena.
75. Wyss, O.A.M. (1932) Winterschlaf und Wärmehaushalt untersucht am Siebenschläfer (Myoxis glis). Pfügers Archiv - European Journal of Physiology, 229, 599-635.