Data logging of body temperatures provides precise information on phenology of reproductive events in a free-living arctic hibernator

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 181, Issue 8, 2011, Pages 1101-1109

  Williams, Cory T ^a,b   Sheriff, Michael J ^a   Schmutz, Joel A ^c   Kohl, Franziska ^a   Tøien, Oivind ^a   Buck, C Loren ^b   Barnes, Brian M ^a  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^b UNIVERSITY OF ALASKA ANCHORAGE   (United States)

^c U S GEOLOGICAL SURVEY   (United States)

Author keywords

Arctic ground squirrels; Biological rhythms; Emergence; Heterothermy; Hibernation; Life history stage; Parturition; Phenological changes

Indexed keywords

ANIMAL; ARTICLE; BIRTH; BODY TEMPERATURE; CIRCADIAN RHYTHM; FEMALE; HIBERNATION; MALE; PERIODICITY; PHYSIOLOGY; PREGNANCY; REPRODUCTION; SCIURIDAE; SEASON; SEXUAL BEHAVIOR; STATISTICAL MODEL;

ANIMALS; BODY TEMPERATURE; CIRCADIAN RHYTHM; FEMALE; HIBERNATION; MALE; MODELS, STATISTICAL; PARTURITION; PERIODICITY; PREGNANCY; REPRODUCTIVE PHYSIOLOGICAL PHENOMENA; SCIURIDAE; SEASONS; SEXUAL BEHAVIOR, ANIMAL;

ANIMALIA; SCIURIDAE; SPERMOPHILUS; SPERMOPHILUS PARRYII;

EID: 81355123366     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-011-0593-z     Document Type: Article

References (53)

1. Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Akademia Kiado, Budapest, pp 267-281.
2. Barnes BM (1989) Freeze avoidance in a mammal: body temperatures below 0°C in an arctic hibernator. Science 244: 1593-1595.
3. Barnes BM (1996) Relationships between hibernation and reproduction in male ground squirrels. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the Cold. University of New England Press, Armidale, pp 71-80.
4. Barnes BM, Kretzmann M, Licht 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.
5. Barnes BM, 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.
6. Boyer BB, Barnes BM (1999) Molecular and metabolic aspects of mammalian hibernation. Bioscience 49: 713-724.
7. Buck CL, Barnes BM (1999a) Annual cycle of body composition and hibernation in free-living arctic ground squirrels. J Mammal 80: 430-442.
8. Buck CL, Barnes BM (1999b) Temperatures of hibernacula and changes in body composition of arctic ground squirrels over winter. J Mammal 80: 1264-1276.
9. Buck CL, Barnes BM (2000) Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. Am J Physiol Regul Integr Comp Physiol 279: R255-R262.
10. Buck CL, Barnes BM (2003) Androgen in free-living arctic ground squirrels: seasonal changes and influence of staged male-male aggressive encounters. Horm Behav 43: 318-326.
11. Buck CL, Breton A, Kohl F, Tøien Ø, Barnes BM (2008) Overwinter body temperature patterns in free-living arctic squirrels (Spermophilus parryii). In: Lovegrove BG, McKechnie AE (eds) Hypometabolism in animals: torpor hibernation and cryobiology. University of KwaZulu-Natal, Pietermaritzburg, pp 317-326.
12. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York.
13. Charbonnel N, Chaval Y, Berthier K, Deter J, Morand S, Palme R, Cosson JF (2008) Stress and demographic decline: a potential effect mediated by impairment of reproduction and immune function in cyclic vole populations. Phys Biochem Zool 81: 63-73.
14. Cranford JA (1978) Hibernation in the western jumping mouse (Zapus princeps). J Mammal 59: 496-509.
15. Dausmann KH (2005) Measuring body temperature in the field-evaluation of external vs. implanted transmitters in a small mammal. J Thermal Biol 30: 195-202.
16. Dausmann KH, Glos J, Ganzhorn J, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429: 825-826.
17. Ewbank R (1969) The fall in rectal temperature seen before parturition in sheep. J Reprod Fertil 19: 569-571.
18. Fewell JE (1995) Body temperature regulation in rats near term of pregnancy. Can J Physiol Pharmacol 73: 364-368.
19. Fietz J, Schlund W, Dausmann KH, Regelmann M, Heldmaier G (2004) Energetic constraints on sexual activity in the male edible dormouse (Glis glis). Oecologia 138: 202-209.
20. Florant GL, Hill V, Ogilvie MD (2000) Circadian rhythms of body temperature in laboratory and field marmots (Marmota flaviventris). In: Heldmaier G, Klingenspor M (eds) Life in the cold: eleventh international hibernation symposium. Springer, Berlin, pp 223-231.
21. Franken RJ, Hik DS (2004) Interannual variation in timing of parturition and growth of collared pikas (Ochotona collaris) in the southwest Yukon. Integr Comp Biol 44: 186-193.
22. Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Ann Rev Physiol 66: 239-274.
23. Gillingham MP, Bunnell FL (1985) Reliability of motion-sensitive collars for estimating activity of black bears. J Wildl Manage 49: 951-958.
24. Gillis EA, Morrisson SF, Zazula GD, Hik DS (2010) Evidence for selective caching by arctic ground squirrels living in alpine meadows in the Yukon. Arctic 58: 354-360.
25. Handrich Y, Bevan RM, Charrassin JB, Butler PJ, Pütz K, Woakes AJ, Lage J, Le Maho Y (1997) Hypothermia in foraging king penguins. Nature 388: 64-67.
26. Hut RA, Barnes BM, Daan S (2002) Body temperature patterns before, during, and after semi-natural hibernation in the European ground squirrel. J Comp Physiol B 172: 47-58.
27. Inouye DW, Barr B, Armitage KB, Inouye BD (2000) Climate change is affecting altitudinal migrants and hibernating species. Proc Natl Acad Sci USA 97: 1630-1633.
28. Karpovich SA, Tøien Ø, Buck CL, Barnes BM (2009) Energetics of arousal episodes in hibernating arctic ground squirrels. J Comp Physiol B 179: 691-700.
29. Kenagy GJ, Sharbaugh SM, Nagy KA (1989) Annual cycle of energy and time expenditure in a golden-mantled ground-squirrel population. Oecologia 78: 269-282.
30. Kenagy GJ, Masman D, Sharbaugh SM, Nagy KA (1990) Energy expenditure during lactation in relation to litter size in free-living golden-mantled ground squirrels. J Anim Ecol 59: 73-88.
31. King GJ, Willoughby RA, Hacker RR (1972) Fluctuations in rectal temperature of swine at parturition. Can Vet J 13: 72-74.
32. Körtner G, Geiser F (1998) Ecology of natural hibernation in the marsupial mountain pygmy-possum (Barramys parvus). Oecologia 113: 170-178.
33. Lacey EA (1991) Reproductive and dispersal strategies of male Arctic ground squirrels (Spermophilus parryii plesius). PhD Thesis, University of Michigan, Ann Arbor, MI, USA.
34. Lammoglia MA, Bellows RA, Short RE, Bellows SE, Bighorn EG, Stevenson JS, Randall RD (1997) Body temperature and endocrine interactions before and after calving in beef cows. J Anim Sci 75: 2526-2534.
35. Long RA, Hut RA, Barnes BM (2007) Simultaneous collection of body temperature and activity data in burrowing mammals: a new technique. J Wildl Manage 71: 1375-1379.
36. Maxwell CS, Morton ML (1975) Thermoregulatory capabilities of neonatal ground squirrels. J Mammal 56: 821-828.
37. McAdam AG, Boutin S (2003) Effects of food abundance on genetic and maternal variation in the growth rate of juvenile red squirrels. J Evol Biol 16: 1249-1256.
38. McLean IG, Towns AJ (1981) Differences in weight changes and the annual cycle of male and female arctic ground squirrels. Arctic 34: 49-254.
39. Michener GR (1992) Sexual differences in over-winter torpor pattern of Richardson's ground squirrels in natural hibernacula. Oecologia 89: 397-406.
40. Michener GR (1993) Sexual differences in hibernaculum contents of Richardson's ground squirrels: males store food. In: Carey C, Florant GL, Wunder BA, Horwitz B (eds) Life in the cold: ecological physiological and molecular mechanisms. Westview Press, Boulder, pp 109-118.
41. Møller AP, Flensted-Jensen E, Klarborg K, Mardal W, Nielsen JT (2010) Climate change affects the duration of reproductive season in birds. J Anim Ecol 79: 777-784.
42. O'Donoghue M, Krebs CJ (1992) Effects of supplemental food on snowshoe hare reproduction and juvenile growth at a cyclic population peak. J Anim Ecol 61: 631-641.
43. Ozgul A, Childs DZ, Oli MK, Armitage KB, Blumstein DT, Olson LE, Tuljapurka S, Coulson T (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature 466: 482-487.
44. Post E, Forchhammer MC (2008) Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Philos Trans R Soc Lond B Biol Sci 363: 2369-2375.
45. Root TL, Price JL, Hall KR, Schneider SH, Rosenzweig C, Pounds AJ (2003) Fingerprints of global warming on wild animals and plants. Nature 421: 57-60.
46. Ruf T (1999) The Lomb-Scargle periodogram in biological rhythm research: analysis of incomplete and unequally spaced time-series. Biol Rhythm Res 30: 178-201.
47. Scribner SJ, Wynne-Edwards KE (1994) Disruption of body temperature and behavior rhythms during reproduction in dwarf hamsters (Phodopus). Physiol Behav 55: 361-369.
48. Serreze MC, Francis JA (2006) The arctic amplification debate. Clim Chang 76: 241-264.
49. Sheriff MJ, Krebs CJ, Boonstra R (2009) The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J Anim Ecol 78: 1249-1258.
50. Sheriff MJ, Kenagy GJ, Richter M, Lee T, Tøien Ø, Kohl F, Buck CL, Barnes BM (2011) Phenological plasticity: variation in annual timing of hibernation and breeding in two nearby populations of arctic ground squirrels. Proc Roy Soc B. doi: 10. 1098/rspb. 2010. 2482.
51. Speakman JR, Król E (2010) Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J Anim Ecol 79: 726-746.
52. Tøien Ø, Blake J, Edgar DM, Grahn DA, Heller HC, Barnes BM (2011) Hibernation in black bears: independence of metabolic suppression from body temperature. Science 331: 906-909.
53. Whidden SE, Williams CT, Breton AR, Buck CL (2007) Effects of transmitters on the reproductive success of tufted puffins. J Field Ornithol 78: 206-212.