Phenology of hibernation and reproduction in ground squirrels: Integration of environmental cues with endogenous programming

Journal of Zoology

Volumn 292, Issue 2, 2014, Pages 112-124

  Williams, C T ^a   Barnes, B M ^b   Kenagy, G J ^c   Buck, C L ^a  

^a UNIVERSITY OF ALASKA ANCHORAGE   (United States)

^b UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Circannual clock; Hibernation; Phenology; Photoperiodism; Sciuridae; Seasonality; Squirrel; Torpor

Indexed keywords

BODY TEMPERATURE; DORMANCY; ENVIRONMENTAL CONDITIONS; HIBERNATION; INTRASPECIFIC VARIATION; METABOLISM; PHENOLOGY; PHENOTYPIC PLASTICITY; PHYSIOLOGY; REPRODUCTION; RODENT; TORPOR;

ANIMALIA; MAMMALIA; MARMOTINI; RODENTIA; SCIURIDAE; SPERMOPHILUS;

EID: 84892871914     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/jzo.12103     Document Type: Article

References (125)

1. Armitage, K.B. (1999). Evolution of sociality in marmots. J. Mammal. 80, 1-10.
2. Armitage, K.B. & Shulenberger, E. (1972). Evidence for a circannual metabolic cycle in Citellus tridecemlineatus. Comp. Biochem. Physiol. 42, 667-688.
3. Arnold, W. (1988). Social thermoregulation during hibernation in alpine marmots (Marmota marmota). J. Comp. Physiol. [B.] 158, 151-156.
4. Arnold, W. (1993). Energetics of social hibernation. In Life in the cold: ecological, physiological, and molecular mechanisms: 65-80. Carey, C., Florant, G.L., Wunder, B.A. & Horwitz, B. (Eds). Boulder: Westview Press.
5. Baker, J.R. (1938). The evolution of breeding seasons. In Evolution: essays on aspects of evolutionary biology, presented to Professor EF Goodrich on his seventieth birthday: 161-177. de Beer, G.R. (Ed.). Oxford: Oxford University Press.
6. Bakko, E.B., Porter, W.P. & Wunder, B.A. (1988). Body temperature patterns in black-tailed prairie dogs in the field. Can. J. Zool. 66, 1783-1789.
7. Barnes, B.M. (1996). Relationships between hibernation and reproduction in male ground squirrels, In Adaptations to the cold. Tenth International Hibernation Symposium: 71-80. Geiser, F., Hulbert, A.J. & Nicol, S.C. (Eds). Armidale: University of New England Press.
8. Barnes, B.M. & Ritter, D. (1993). Patterns of body temperature change in hibernating arctic ground squirrels. In Life in the cold: ecological, physiological, and molecular mechanisms: 119-130. Carey, C., Florant, G.L., Wunder, B.A. & Horwitz, B. (Eds). Boulder: Westview Press.
9. Barnes, B.M. & York, A.D. (1990). Effect of winter high temperatures on reproduction and circannual rhythms in hibernating ground squirrels. J. Biol. Rhythms 5, 119-130.
10. Barnes, B.M., Kretzmann, M., Light, P. & Zucker, I. (1986). The influence of hibernation on testis growth and spermatogenesis in the golden-mantled ground squirrel, Spermophilus lateralis. Biol. Reprod. 35, 1289-1297.
11. Barnes, B.M., Licht, P. & Zucker, I. (1987). Temperature dependence of in vitro androgen production in testes from hibernating ground squirrels, Spermophilus lateralis. Can. J. Zool. 65, 3020-3023.
12. Barnes, B.M., Kretzmann, M., Zucker, I. & Licht, P. (1988). Plasma androgen and gonadotropin levels during hibernation and testicular maturation in golden-mantled ground squirrels. Biol. Reprod. 38, 616-622.
13. Bieber, C., Juškaitis, R., Turbill, C. & Ruf, T. (2012). High survival during hibernation affects onset and timing of reproduction. Oecologia 169, 155-166.
14. Blumstein, D.T. (2009). Social effects on emergence from hibernation in yellow-bellied marmots. J. Mammal. 90, 1184-1187.
15. Blumstein, D.T., Im, S., Nicodemus, A. & Zugmeyer, C. (2004). Yellow-bellied marmots (Marmota flaviventris) hibernate socially. J. Mammal. 85, 25-29.
16. Boyce, M.S. (1979). Seasonality and patterns of natural selection for life histories. Am. Nat. 114, 569-583.
17. Bradshaw, W.E. & Holzapfel, C.M. (2007). Evolution of animal photoperiodism. Annu. Rev. Ecol. Evol. Syst. 38, 1-25.
18. Brigham, R.M. & Geiser, F. (2012). Do red squirrels (Tamiasciurus hudsonicus) use daily torpor during winter? Ecoscience 19, 127-132.
19. Broadbooks, H.E. (1958). Life history and ecology of the chipmunk, Eutamias amoenus, in Eastern Washington. Misc. Publ., Mus. Zool., Univ. Michigan 103, 1-42.
20. Bronson, M.T. (1980). Altitudinal variation in emergence time of golden-mantled ground squirrels (Spermophilus lateralis). J. Mammal. 61, 124-126.
21. Buck, C.L. & Barnes, B.M. (1999a). Annual cycle of body composition and hibernation in free-living arctic ground squirrels. J. Mammal. 80, 430-442.
22. Buck, C.L. & Barnes, B.M. (1999b). Temperatures of hibernacula and changes in body composition of arctic ground squirrels over winter. J. Mammal. 80, 1264-1276.
23. Buck, C.L. & Barnes, B.M. (2003). Androgen in free-living arctic ground squirrels: seasonal changes and influence of staged male-male aggressive encounters. Horm. Behav. 43, 318-326.
24. Buhr, E.D., Seung-Hee, Y. & Takahashi, J.S. (2010). Temperature as a universal resetting cue for mammalian circadian oscillators. Science 330, 379-385.
25. Carmichael, M.S. & Zucker, I. (1986). Circannual rhythms of ground squirrels: a test of the frequency demultiplication hypothesis. J. Biol. Rhythms 1, 277-284.
26. Clements, M.N., Clutton-Brock, T.H., Albon, S.D., Pemberton, J.M. & Kruuk, L.E.B. (2010). Getting the timing right: antler growth phenology and sexual selection in a wild red deer population. Oecologia 164, 357-368.
27. Coulson, S.J., Hodkinson, I.D., Strathdee, A.T., Block, W., Webb, N.R., Bale, J.S. & Worland, M.R. (1995). Thermal environments of arctic soil organisms during winter. Arct. Alp. Res. 27, 364-370.
28. Dardente, H. (2012). Melatonin-dependent timing of seasonal reproduction by the pars tuberalis: pivotal roles for long daylengths and thyroid hormones. J. Neuroendocrinology 24, 249-266.
29. Dark, J., Miller, D.R. & Zucker, I. (1996). Gonadectomy in the spring reinstates hibernation in male golden-mantled ground squirrels. Am. J. Physiol. Regul. Integr. Comp. Physiol. 270, R1240-R1243.
30. Dausmann, K.H., Wein, J., Turner, J.M. & Glos, J. (2013). Absence of heterothermy in the European red squirrel (Sciurus vulgaris). Mamm. Biol. 78, 332-335.
31. Davis, D.E. (1967). The annual rhythm of fat deposition in woodchucks (Marmota monax). Physiol. Zool. 40, 391-402.
32. Dibner, C., Schibler, U. & Albrecht, U. (2010). The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72, 517-549.
33. Florant, G.L. & Healy, J.E. (2012). The regulation of food intake in mammalian hibernators: a review. J. Comp. Physiol. [B.] 182, 451-567.
34. French, A.R. (2000). Interdependency of stored food and changes in body temperature during hibernation of the eastern chipmunk, Tamias striatus. J. Mammal. 81, 979-985.
35. Garland, T. & Adolph, S.C. (1991). Physiological differentiation of vertebrate populations. Annu. Rev. Ecol. Syst. 22, 193-228.
36. Geiser, F. (2004). Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66, 239-274.
37. 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.
38. Geiser, F., Hiebert, S. & Kenagy, G.J. (1990). Torpor bout duration during the hibernation season of two sciurid rodents: interrelations with temperature and metabolism. Physiol. Zool. 63, 489-503.
39. Geiser, F., McAllan, B.M. & Kenagy, G.J. (1994). The degree of dietary fatty acid unsaturation affects torpor patterns and lipid composition of a hibernator. J. Comp. Physiol. [B.] 164, 299-305.
40. Gillis, E.A., Morrison, S.F., Zazula, G.D. & Hik, D.S. (2005). Evidence for selective caching by arctic ground squirrels living in alpine meadows in the Yukon. Arctic 58, 354-360.
41. Golombek, D.A. & Rosenstein, R.E. (2010). Physiology of circadian entrainment. Physiol. Rev. 90, 1063-1102.
42. Gwinner, E. (1973). Circannual rhythyms in birds: their interaction with circadian rhythms and environmental photoperiod. J. Reprod. Fertil. 19, 51-65.
43. Gwinner, E. (1986). Circannual rhythms. Heidelberg: Springer.
44. Hanon, E.A., Routledge, K., Dardente, H., Masson-Pévet, M., Morgan, P.J. & Hazlerigg, D.G. (2010). Effect of photoperiod on the thyroid-stimulating hormone neuroendocrine system in the European hamster (Cricetus cricetus). J. Neuroendocrinol. 22, 51-55.
45. Hansen, M.M., Olivieri, I., Waller, D.M. & Nielsen, E.E. (2012). Monitoring adaptive genetic responses to environmental change. Mol. Ecol. 21, 1311-1329.
46. Harlow, H.J. & Menkens, G.E. Jr. (1986). A comparison of hibernation in the black-tailed prairie dog, white-tailed prairie dog, and Wyoming ground squirrel. Can. J. Zool. 64, 793-796.
47. Hazlerigg, D.G. & Lincoln, G.A. (2011). Hypothesis: cyclical histogenesis is the basis of circannual timing. J. Biol. Rhythms 26, 471-485.
48. Hazlerigg, D.G. & Loudon, A. (2008). New insights into ancient seasonal life timers. Curr. Biol. 18, R795-R804.
49. Healy, J.E., Burdett, K.A., Buck, C. & Florant, G.L. (2012). Sex differences in torpor patterns during natural hibernation in golden-mantled ground squirrels (Callospermophilus lateralis). J. Mammal. 93, 751-758.
50. Heller, H.C. & Poulson, T.L. (1970). Circannian rhythms II: endogenous and exogenous factors controlling reproduction and hibernation in chipmunks (Eutamias) and ground squirrels (Spermophilus). Comp. Biochem. Physiol. 33, 357-383.
51. Holekamp, K.E. & Nunes, S. (1989). Seasonal variation in body weight, fat, and behavior of California ground squirrels (Spermophilus beecheyi). Can. J. Zool. 67, 1425-1433.
52. Holekamp, K.E. & Talamantes, F. (1991). Seasonal variation in circulating testosterone and oestrogens of wild-caught California ground squirrels (Spermophilus beecheyi). J. Reprod. Fertil. 93, 415-425.
53. Humphries, M.M., Thomas, D.W., Hall, C.L., Speakman, J.R. & Kramer, D.L. (2002). The energetics of autumn mast hoarding in eastern chipmunks. Oecologia 133, 30-37.
54. Humphries, M.M., Kramer, D.L. & Thomas, D.W. (2003). The role of energy availability in mammalian hibernation: an experimental test in free-ranging eastern chipmunks. Physiol. Biochem. Zool. 76, 180-186.
55. Humphries, M.M., Boutin, S., Thomas, D.W., Ryan, J.D., Selman, C., McAdam, A.G., Berteaux, D. & Speakman, J.R. (2005). Expenditure freeze: the metabolic response of small mammals to cold environments. Ecol. Lett. 8, 1326-1333.
56. Hut, R.A., van Oort, B.E. & Daan, S. (1999). Natural entrainment without dawn and dusk: the case of the European ground squirrel (Spermophilus citellus). J. Biol. Rhythms 14, 290-299.
57. Ikegami, K. & Yoshimura, T. (2012). Circadian clocks and the measurement of daylength in seasonal reproduction. Mol. Cell. Endocrinol. 349, 76-81.
58. Inouye, D.W., Barr, B., Armitage, K.B. & Inouye, B.D. (2000). Climate change is affecting altitudinal migrants and hibernating species. Proc. Natl. Acad. Sci. U.S.A. 97, 1630-1633.
59. Iverson, S.L. & Turner, B.N. (1972). Natural history of a Manitoba population of Franklin's ground squirrel. Can. Field Nat. 86, 145-149.
60. Kawamichi, M. (1996). Ecological factors affecting annual variation in commencement of hibernation in wild chipmunks (Tamias sibiricus). J. Mammal. 77, 731-744.
61. Kenagy, G.J. (1980). Interrelation of endogenous annual rhythms of reproduction and hibernation in the golden-mantled ground squirrel. J. Comp. Physiol. [A.] 135, 333-339.
62. Kenagy, G.J. (1981a). Endogenous annual rhythm of reproductive function in the non-hibernating desert ground squirrel Ammospermophihis leucurus. J. Comp. Physiol. 142, 251-258.
63. Kenagy, G.J. (1981b). Effects of day length, temperature, and endogenous control on annual rhythms of reproduction and hibernation in chipmunks (Eutamias ssp.) J. Comp. Physiol. [A.] 141, 369-378.
64. Kenagy, G.J. & Barnes, B.M. (1988). Seasonal reproductive patterns in four coexisting rodent species from the Cascade Mountains, Washington. J. Mammal. 69, 274-292.
65. Kenagy, G.J. & Bartholomew, G.A. (1979). Effects of day length and endogenous control on the annual reproductive cycle of the antelope ground squirrel, Ammospermophilus leucurus. J. Comp. Physiol. 130, 131-136.
66. Knopf, F.L. & Balph, D.F. (1977). Annual periodicity of Uinta ground squirrels. Southwest. Nat. 22, 213-224.
67. Körtner, G. & Geiser, F. (2000). The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol. Int. 17, 103-128.
68. Lacey, E.A. (1991). Reproductive and dispersal strategies of male Arctic ground squirrels (Spermophilus parryii plesius). PhD thesis, University of Michigan, Ann Arbor, MI, USA.
69. Lande, R. & Shannon, S. (1996). The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50, 434-437.
70. Landry-Cuerrier, M., Munro, D., Thomas, D.W. & Humphries, M.M. (2008). Climate and resource determinants of fundamental and realized metabolic niches of hibernating chipmunks. Ecology 89, 3306-3316.
71. Lane, J.E. (2012). Evolutionary ecology of mammalian hibernation phenology. In Living in a seasonal world: thermoregulatory and metabolic adaptations: 51-61. Ruf, T., Bieber, C., Arnold, W. & Millesi, E. (Eds). Berlin: Springer-Verlag.
72. Lane, J.E., Kruuk, L.E.B., Charmantier, A., Murie, J.O., Coltman, D.W., Buoro, M., Raveh, S. & Dobson, F.S. (2011). A quantitative genetic analysis of hibernation emergence date in a wild population of Columbian ground squirrels. J. Evol. Biol. 24, 1949-1959.
73. Lane, J.E., Kruuk, L.E.B., Charmantier, A., Murie, J.O. & Dobson, F.S. (2012). Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 489, 554-557.
74. Lee, T.M. & Zucker, I. (1991). Suprachiasmatic nucleus and photic entrainment of circannual rhythms in ground squirrels. J. Biol. Rhythms 6, 315-330.
75. Lee, T.M., Pelz, K., Licht, P. & Zucker, I. (1990). Testosterone influences hibernation in golden-mantled ground squirrels. Am. J. Physiol. Regul. Integr. Comp. Physiol. 259, R760-R767.
76. Lee, T.N., Barnes, B.M. & Buck, C.L. (2009). Body temperature patterns during hibernation in a free-living Alaska marmot (Marmota broweri). Ethol. Ecol. Evol. 21, 403-413.
77. Lehmer, E.M., Savage, L.T., Antolin, M.F. & Biggins, D.E. (2006). Extreme plasticity in thermoregulatory behaviors of free-ranging black-tailed prairie dogs. Physiol. Biochem. Zool. 79, 454-467.
78. Liedvogel, M., Szulkin, M., Knowles, S.C., Wood, M.J. & Sheldon, B.C. (2009). Phenotypic correlates of Clock gene variation in a wild blue tit population: evidence for a role in seasonal timing of reproduction. Mol. Ecol. 18, 2444-2456.
79. Lincoln, G.A., Johnston, J.D., Andersson, H., Wagner, G. & Hazlerigg, D.G. (2005). Photorefractoriness in mammals: dissociating a seasonal timer from the circadian-based photoperiod response. Endocrinology 146, 3782-3790.
80. Lincoln, G.A., Clarke, I.J., Hut, R.A. & Hazlerigg, D.G. (2006). Characterizing a mammalian circannual pacemaker. Science 314, 1941-1944.
81. Ling, F. & Zhang, T. (2003). Impact of the timing and duration of seasonal snow cover on the active layer and permafrost in the Alaskan Arctic. Permafrost Periglac. Process. 14, 141-150.
82. Michener, G.R. (1977). Effect of climatic conditions on the annual activity and hibernation cycle of Richardson's ground squirrels and Columbian ground squirrels. Can. J. Zool. 55, 693-703.
83. Michener, G.R. (1979). The circannual cycle of Richardson's ground squirrels in southern Alberta. J. Mammal. 60, 760-768.
84. Michener, G.R. (1983). Spring emergence schedules and vernal behavior of Richardson's ground squirrels: why do males emerge from hibernation before females? Behav. Ecol. Sociobiol. 14, 29-38.
85. Michener, G.R. (1984). Age, sex, and species differences in the annual cycles of ground-dwelling sciurids. In The biology of the ground-dwelling squirrels: annual cycles, behavioral ecology, and sociality: 81-107. Murie, J.O. & Michener, G.R. (Eds). Lincoln: University of Nebraska Press.
86. Michener, G.R. (1992). Sexual differences in over-winter torpor patterns of Richardson's ground squirrels in natural hibernacula. Oecologia 89, 397-406.
87. Millesi, E., Strijkstra, A.M., Hoffmann, I.E., Dittami, J.P. & Daan, S. (1999). Sex and age differences in mass, morphology, and annual cycle in European ground squirrels, Spermophilus citellus. J. Mammal. 80, 218-231.
88. Morrow, G. & Nicol, S.C. (2009). Cool sex? Hibernation and reproduction overlap in the echidna. PLoS ONE 4, e6070.
89. Morton, M.L. & Sherman, P.W. (1978). Effects of a spring snowstorm on behavior, reproduction, and survival of Belding's ground squirrels. Can. J. Zool. 56, 2578-2590.
90. Mrosovsky, N. (1971). Hibernation and the hypothalamus. New York: Springer.
91. Munro, D., Thomas, D.W. & Humphries, M.M. (2005). Torpor patterns of hibernating eastern chipmunks Tamias striatus vary in response to the size and fatty acid composition of food hoards. J. Anim. Ecol. 74, 692-700.
92. Munro, D., Thomas, D.W. & Humphries, M.M. (2008). Extreme suppression of aboveground activity by a food-storing hibernator, the eastern chipmunk (Tamias striatus). Can. J. Zool. 86, 364-370.
93. Murie, J.O. & Harris, M.A. (1982). Annual variation of spring emergence and breeding in Columbian ground squirrels (Spermophilus columbianus). J. Mammal. 63, 431-439.
94. Neuhaus, P. (2000). Timing of hibernation and molt in female Columbian ground squirrels. J. Mammal. 81, 571-577.
95. Ozgul, A., Childs, D.Z., Oli, M.K., Armitage, K.B., Blumstein, D.T., Olson, L.E., Tuljapurkar, S. & Coulson, T. (2010). Coupled dynamics of body mass and population growth in response to environmental change. Nature 466, 482-485.
96. Parmesan, C. & Yohe, G. (2003). A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37-42.
97. Pengelley, E.T. & Fisher, K.C. (1963). The effect of temperature and photoperiod on the yearly hibernating behavior of captive golden-mantled ground squirrels (Citellus lateralis tescorum). Can. J. Zool. 41, 1103-1120.
98. Pengelley, E.T., Asmundson, S.J., Barnes, B. & Aloia, R.C. (1976). Relationship of light intensity and photoperiod to circannual rhythmicity in the hibernating ground squirrel, Citellus lateralis. Comp. Biochem. Physiol. A 53, 273-277.
99. Place, N.J., Veloso, C., Visser, G.H. & Kenagy, G.J. (2002). Energy expenditure and testosterone in free-living male yellow-pine chipmunks. J. Exp. Zool. 292, 460-467.
100. Przybylo, R., Sheldon, B.C. & Merilä, J. (2000). Climatic effects on breeding and morphology: evidence for phenotypic plasticity. J. Anim. Ecol. 69, 395-403.
101. Ruf, T. & Arnold, W. (2008). Effects of polyunsaturated fatty acids on hibernation and torpor: a review and hypothesis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1044-R1052.
102. Shaw, W.T. (1925). The seasonal differences of north and south slopes in controlling the activities of the Columbian ground squirrel. Ecology 6, 157-163.
103. Sheriff, M.J., Kenagy, G.J., Richter, M., Lee, T., Tøien, Ø., Kohl, F., Buck, C.L. & Barnes, B.M. (2011). Phenological variation in annual timing of hibernation and breeding in nearby populations of arctic ground squirrels. Proc. Biol. Sci. 278, 2369-2375.
104. Smith, G.W. & Johnson, D.R. (1985). Demography of a Townsend ground squirrel population in southwestern Idaho. Ecology 66, 171-178.
105. Snyder, R.L. & Christian, J.J. (1960). Reproductive cycle and litter size of the woodchuck. Ecology 41, 647-656.
106. Sumová, A., Jáč, M., Sládek, M., Šauman, I. & Illnerová, H. (2003). Clock gene daily profiles and their phase relationship in the rat suprachiasmatic nucleus are affected by photoperiod. J. Biol. Rhythms 18, 134-144.
107. Thackeray, S.J., Sparks, T.H., Frederiksen, M., Burthe, S., Bacon, P.J., Bell, J.R., Botham, M.S., Brereton, T.M., Bright, P.W., Carvalho, L., Clutton-Brock, T., Dawson, A., Edwards, M., Elliot, J.M., Harrington, R., Jhons, D., Jones, I.D., Jones, J.T., Leech, D.I., Roy, D.B., Scott, W.A., Smith, M., Smithers, R.J., Winfield, I.J., Wanless, S. (2010). Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob. Change Biol. 16, 3304-3313.
108. Tournier, B.B., Menet, J.S., Dardente, H., Poirel, V.J., Malan, A., Masson-Pevet, M., Pevet, P. & Vuillez, P. (2003). Photoperiod differentially regulates clock genes' expression in the suprachiasmatic nucleus of Syrian hamster. Neuroscience 118, 317-322.
109. Turbill, C., Bieber, C. & Ruf, T. (2011). Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc. Biol. Sci. 278, 3355-3363.
110. Visser, M.E. (2008). Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc. Biol. Sci. 275, 649-659.
111. Visser, M.E. & Both, C. (2005). Shifts in phenology due to global climate change: the need for a yardstick. Proc. Biol. Sci. 272, 2561-2569.
112. Wade, O. (1950). Soil temperatures, weather conditions, and emergence of ground squirrels from hibernation. J. Mammal. 31, 158-161.
113. Ward, J.M. & Armitage, K.B. (1981). Circannual rhythms of food consumption, body mass, and metabolism in yellow-bellied marmots. Comp. Biochem. Physiol. A 69, 621-626.
114. Wikelski, M., Martin, L.B., Scheuerlein, A., Robinson, M.T., Robinson, N.D., Helm, B., Hau, M. & Gwinner, E. (2008). Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control. Philos. Trans. R. Soc. Lond. B. Biol Sci. 363, 411-423.
115. Williams, C.T., Sheriff, M.S., Schmutz, J.A., Kohl, F., Tøien, Ø., Buck, C.L. & Barnes, B.M. (2011). Data logging of body temperatures provides precise information on phenology of reproductive events in a free-living arctic hibernator. J. Comp. Physiol. [B.] 181, 1101-1109.
116. Williams, C.T., Barnes, B.M. & Buck, C.L. (2012a). Daily body temperature rhythms persist under the midnight sun but are absent during hibernation in free-living arctic ground squirrels. Biol. Lett. 8, 31-34.
117. Williams, C.T., Barnes, B.M., Richter, M. & Buck, C.L. (2012b). Hibernation and circadian rhythms of body temperature in free-living arctic ground squirrels. Physiol. Biochem. Zool. 85, 397-404.
118. Williams, C.T., Sheriff, M.J., Kohl, F., Barnes, B.M. & Buck, C.L. (2012c). Interrelationships among timing of hibernation, reproduction, and warming soil in free-living female arctic ground squirrels. In Living in a seasonal world: thermoregulatory and metabolic adaptations: 63-72. Ruf, T., Bieber, C., Arnold, W. & Millesi, E. (Eds). Berlin: Springer-Verlag.
119. Willis, C.K., Brigham, R.M. & Geiser, F. (2006). Deep, prolonged torpor by pregnant, free-ranging bats. Naturwissenschaften 93, 80-83.
120. Woods, B.C. & Armitage, K.B. (2003). Effect of food supplementation on juvenile growth and survival in Marmota flaviventris. J. Mammal. 84, 903-914.
121. Young, P.J. (1990a). Hibernating patterns of free-ranging Columbian ground squirrels. Oecologia 83, 504-511.
122. Young, P.J. (1990b). Structure, location and availability of hibernacula of Columbian ground squirrels (Spermophilus columbianus). Am. Midl. Nat. 123, 357-364.
123. Zazula, G.D., Mathewes, R.W. & Harestad, A.S. (2006). Cache selection by arctic ground squirrels inhabiting boreal-steppe meadows of southwest Yukon Territory, Canada. Arct. Antarct. Alp. Res. 38, 631-638.
124. Zervanos, S. & Salsbury, C.M. (2003). Seasonal body temperature fluctuations and energetic strategies in free-ranging eastern woodchucks (Marmota monax). J. Mammal. 84, 299-310.
125. Zervanos, S.M., Maher, C.R., Waldvogel, J.A. & Florant, G.L. (2010). Latitudinal differences in the hibernation characteristics of woodchucks (Marmota monax). Physiol. Biochem. Zool. 83, 135-141.