The cold shoulder: Free-ranging snowshoe hares maintain a low cost of living in cold climates

Canadian Journal of Zoology

Volumn 87, Issue 10, 2009, Pages 956-964

  Sheriff, Michael J ^a,b   Speakman, J R ^c   Kuchel, L ^a   Boutin, S ^d   Humphries, M M ^e  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d UNIVERSITY OF ALBERTA   (Canada)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIORAL RESPONSE; COLD AIR; ENDOTHERMY; HYPOTHESIS TESTING; LAGOMORPH; METABOLISM; RESOURCE SCARCITY;

CANADA; NORTH AMERICA; YUKON TERRITORY;

AVES; HYDROMETRIDAE; LEPUS AMERICANUS; MAMMALIA;

EID: 71449104282     PISSN: 00084301     EISSN: None     Source Type: Journal    
DOI: 10.1139/Z09-087     Document Type: Article

References (56)

1. Anderson, K.J., and Jetz, W. 2005. The broad-scale ecology of energy expenditure of endotherms. Ecol. Lett. 8(3): 310-318. doi:10.1111/j.1461-0248.2005.00723.x.
2. Bakken, G.S. 1992. Measurement and application of operative and standard operative temperatures in ecology. Am. Nat. 32: 194-216.
3. Berteaux, D., Thomas, D.W., Bergeron, J.-M., and Lapierre, H. 1996. Repeatability of daily field metabolic rate in female Meadow Voles (Microus pennsylvanicus). Funct. Ecol. 10(6): 751-759. doi:10.2307/2390510.
4. Bozinovic, F., Bacigalupe, L.D., Vásquez, R.A., Visser, G.H., Veloso, C., and Kenagy, G.J. 2004. Cost of living in free-ranging degus (Octodon degus): seasonal dynamics of energy expenditure. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 137(3): 597-604. doi:10.1016/j.cbpb.2003.11.014.
5. Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M., and West, G.B. 2004. Towards a metabolic theory of ecology. Ecology, 85(7): 1771-1789. doi:10.1890/03-9000.
6. Bryant, D.M. 1997. Energy expenditure in wild birds. Proc. Nutr. Soc. 56(3): 1025-1039. doi:10.1079/PNS19970107. PMID: 9483668.
7. Butler, P.J., Green, J.A., Boyd, I.L., and Speakman, J.R. 2004. Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods. Funct. Ecol. 18(2): 168-183. doi:10.1111/j.0269-8463.2004.00821.x.
8. Clarke, A., and Gaston, K.J. 2006. Climate, energy and diversity. Proc. R. Soc. Lond. B Biol. Sci. 273(1599): 2257-2266. doi:10. 1098/rspb.2006.3545.
9. Corp, N., Gorman, M.L., and Speakman, J.R. 1999. Daily energy expenditure of free-living male wood mice in different habitats and seasons. Funct. Ecol. 13(5): 585-593. doi:10.1046/j.1365-2435.1999.00353.x.
10. Covell, D.F., Miller, D.S., and Karasov, W.H. 1996. Cost of locomotion and daily energy expenditure by free-living swift foxes (Vulpes velox): a seasonal comparison. Can. J. Zool. 74(2): 283-290. doi:10.1139/z96-035.
11. Degen, A.A., Khokhlova, I.S., Kam, M., and Nagy, K.A. 1997. Body size, granivory and seasonal dietary shifts in desert gerbilline rodents. Funct. Ecol. 11(1): 53-59. doi:10.1046/j.1365-2435.1997.00059.x.
12. Feist, D.D., and Rosenmann, M. 1975. Seasonal sympatho-adrenal and metabolic responses to cold in the Alaskan snowshoe hare (Lepus americanus macfarlani). Comp. Biochem. Physiol. A Physiol. 51(2): 449-455. doi:10.1016/0300-9629(75)90393-X.
13. Fuglei, E., and Oritsland, N.A. 1999. Seasonal trends in body mass, food intake and resting metabolic rate, and induction of metabolic depression in arctic foxes (Alopex lagopus) at Svalbard. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 169(6): 361-369. PMID:10549138.
14. Fuglesteg, B.N., Haga, O.E., Folkow, L.P., Fuglei, E., and Blix, A.S. 2006. Seasonal variations in basal metabolic rate, lower critical temperature and responses to temporary starvation in the arctic fox (Alopex lagopus) from Svalbard. Polar Biol. 29(4): 308-319. doi:10.1007/s00300-005-0054-9.
15. Hind, A.T., and Gurney, W.S.C. 1998. Are there thermoregulatory constraints on the timing of pupping for harbour seals? Can. J. Zool. 76(12): 2245-2254. doi:10.1139/cjz-76-12-2245.
16. Holleman, D.F., White, R.G., and Feist, D.D. 1982. Seasonal energy and water metabolism in free-living Alaskan voles. J. Mammal. 63(2): 293-296. doi:10.2307/1380640.
17. Humphries, M.M., Boutin, S., Thomas, D.W., Ryan, J.D., Selman, C., McAdam, A.G., Berteaux, D., and Speakman, J.R. 2005. Expenditure freeze: the metabolic response of small mammals to cold environments. Ecol. Lett. 8(12): 1326-1333 doi:10.1111/j. 1461-0248.2005.00839.x.
18. Koteja, P. 1991. On the relation between basal and field metabolic rates in birds and mammals. Funct. Ecol. 5(1): 56-64. doi:10. 2307/2389555.
19. Koteja, P. 1996. Measuring energy metabolism with open-flow respirometric systems: which design to choose? Funct. Ecol. 10(5): 675-677. doi:10.2307/2390179.
20. Krebs, C.J., Gilbert, B.S., Boutin, S., Sinclair, A.R.E., and Smith, J.N.M. 1986. Population biology of snowshoe hares. I. Demography of food-supplemented populations in the southern Yukon, 1976-84. J. Anim. Ecol. 55(3): 963-982. doi:10.2307/4427.
21. Krebs, C.J., Boutin, S., and Boonstra, R. 2001. Ecosystem dynamics of the Boreal Forest: The Kluane Project. Oxford University Press, New York.
22. Masman, D., Daan, S., and Dijkstra, C. 1988. Time allocation in the kestrel (Falco tinnunculus) and the principle of energy minimization. J. Anim. Ecol. 57(2): 411-432. doi:10.2307/4914.
23. Mortensen, A., and Blix, A.S. 1986. Seasonal change in metabolic rate and mass-specific conductance in Svalbard ptarmigan Norwegian rock ptarmigan and Norwegian willow ptarmigan. Ornis Scand. 17(1): 8-13. doi:10.2307/3676746.
24. Mutze, G.J., Green, B., and Newgrain, K. 1991. Water flux and energy use in wild house mice (Mus domesticus) and the impact of seasonal aridity on breeding and population levels. Oecologia (Berl.), 88: 529-538.
25. 18O) Method: a guide to its use. Publ. No. 12-1417, University of California at Los Angeles, Los Angeles.
26. Nagy, K.A. 1994. Field bioenergetics of mammals - what determines field metabolic rates. Aust. J. Zool. 42(1): 43-53. doi:10. 1071/ZO9940043.
27. Nagy, K.A. 2005. Field metabolic rate and body size. J. Exp. Biol. 208(9): 1621-1625. doi:10.1242/jeb.01553. PMID:15855393.
28. Nagy, K.A., and Gruchacz, M.J. 1994. Seasonal water and energy metabolism of the desert dwelling kangaroo rat (Dipodomys merriami). Physiol. Zool. 67: 1461-1478.
29. Nagy, K.A., Girard, I.A., and Brown, T.K. 1999. Energetics of free-ranging mammals, reptiles, and birds. Annu. Rev. Nutr. 19(1): 247-277. doi:10.1146/annurev.nutr.19.1.247. PMID: 10448524.
30. Nassuna-Musoke, G.M., Kabassa, J.D., and King, M.J. 2007. Response of Friesian cows to microclimate on small farms in warm tropical climates. J. Anim. Vet. Adv. 6: 899-906.
31. Nilssen, K.J., Sundsfjord, J.A., and Blix, A.S. 1984. Regulation of metabolic rate in Svalbard and Norwegian reindeer. Am. J. Physiol. 247(5 Pt 2): R837-R841. PMID:6496770.
32. Nolet, B.A., and Rosell, F. 1994. Territoriality and time budgets in beavers during sequential settlement. Can. J. Zool. 72(7): 1227-1237. doi:10.1139/z94-164.
33. Ochociń D., and Taylor, J.R.E. 2005. Living at the physiological limits: field and maximum metabolic rates of the common shrew (Sorex araneus). Physiol. Biochem. Zool. 78(5): 808-818. doi:10.1086/431190. PMID:16096983.
34. Pauls, R.W. 1978. Behavioural strategies relevant to the energy economy of the red squirrel (Tamiasciurus hudsonicus). Can. J. Zool. 56(7): 1519-1525. doi:10.1139/z78-210.
35. R Development Core Team. 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.r-project.org/.
36. Redman, P., Selman, C., and Speakman, J.R. 1999. Male shorttailed field voles (Microtus agrestis) build better insulated nests than females. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 169: 581-587.
37. Rosenmann, M., Morrison, P., and Feist, D.D. 1975. Seasonal changes in the metabolic capacity of red-backed voles. Physiol. Zool. 48: 303-310.
38. Scholander, P.F. 1955. Evolution of climatic adaptation in homeotherms. Evolution, 9(1): 15-26. doi:10.2307/2405354.
39. Scholander, P.F., Walters, V., Hock, R., and Irving, L. 1950a. Body insulation of some arctic and tropical mammals and birds. Biol. Bull. (Woods Hole), 99(2): 225-236. doi:10.2307/1538740. PMID:14791421.
40. Scholander, P.F., Hock, R., Walters, V., and Irving, L. 1950b. Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. Biol. Bull. (Woods Hole), 99(2): 259-271. doi:10.2307/1538742. PMID:14791423.
41. Sheriff, M.J., Krebs, C.J., and Boonstra, R. 2009a. The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J. Anim. Ecol. In press. doi:10.1111/j.1365 2656.2009.01552.x.
42. Sheriff, M.J., Kuchel, L., Boutin, S., and Humphries, M.M. 2009b. Seasonal metabolic acclimatization in a northern population of free-ranging snowshoe hares, Lepus americanus. J. Mammal. 90(3): 761-767. doi:10.1644/08-MAMM-A-247R.1.
43. Shoemaker, V.H., Nagy, K.A., and Costa, W.R. 1976. Energy utilization and temperature regulation by jackrabbits (Lepus californicus) in the Mojave Desert. Physiol. Zool. 49: 364-375.
44. Sinclair, A.R.E., Krebs, C.J., and Smith, J.N.M. 1982. Diet quality and food limitation in herbivores: the case of the snowshoe hare. Can. J. Zool. 60(5): 889-897. doi:10.1139/z82-121.
45. 2 production in doubly labelled water studies of animals? Funct. Ecol. 7: 746-750.
46. Speakman, J.R. 1997. Doubly labelled water: theory and practice. Chapman and Hall, London.
47. Speakman, J.R. 1998. The history and theory of the doubly labeled water technique. Am. J. Clin. Nutr. 68(4): 932S-938S. PMID: 9771875.
48. Speakman, J.R. 1999. The cost of living: field metabolic rates of small mammals. Adv. Ecol. Res, 30: 177-297 doi:10.1016/S0065-2504(08)60019-7.
49. Speakman, J.R., and Król, E. 2005. Comparison of different ap-proaches for the calculation of energy expenditure using doubly labeled water in a small mammal. Physiol. Biochem. Zool. 78: 650-667 doi:10.1086/430234. PMID:15957119.
50. Speakman, J.R., and Racey, P.A. 1987. The equilibrium concentration of oxygen-18 in body water: implications for the accuracy of the doubly-labelled water technique and a potential new method of measuring RQ in free-living animals. J. Theor. Biol. 127(1): 79-95. doi:10.1016/S0022-5193(87)80162-5.
51. 2 production for accuracy of the doubly labelled water technique: the importance of recapture interval. Comp. Biochem. Physiol. A Physiol. 90(2): 337-340. doi:10.1016/0300-9629(88)91125-5.
52. Speakman, J.R., Racey, P.A., Haim, A., Webb, P.I., Ellison, G.T.H., and Skinner, J.D. 1994. Interand intraindividual variation in daily energy expenditure of the pouched mouse (Saccostomus campestris). Funct. Ecol. 8(3): 336-342. doi:10.2307/2389826.
53. Steel, M.A. 1998. Tamiasciurus hudsonicus. Mamm. Species, 586: 1-9.
54. Van Trigt, R., Kerstel, E.R.T., Neubert, R.E.M., Meijer, H.A.J., McLean, M., and Visser, G.H. 2002. Validation of the DLW method in Japanese quail at different water fluxes using laser and IRMS. J. Appl. Physiol. 93(6): 2147-2154. PMID:12433938.
55. Visser, G.H., and Schekkerman, H. 1999. Validation of the doubly labeled water method in growing precocial birds: the importance of assumptions concerning evaporative water loss. Physiol. Biochem. Zool. 72(6): 740-749. doi:10.1086/316713. PMID: 10603338.
56. Weiner, J. 1992. Physiological limits to sustainable energy budgets in birds and mammals. Trends Ecol. Evol. 7(11): 384-388. doi:10.1016/0169-5347(92)90009-Z.