Of lemmings and snowshoe hares: The ecology of northern Canada

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1705, 2011, Pages 481-489

  Krebs, Charles J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Food shortage; Lemmings; Maternal effects; Predation; Snowshoe hares; Social mortality

Indexed keywords

BOREAL FOREST; FOOD LIMITATION; LAGOMORPH; MATERNAL EFFECT; MORTALITY; PERIODICITY; POPULATION DENSITY; POPULATION GROWTH; PREDATION RISK; RODENT; TERRESTRIAL ECOSYSTEM;

CANADA;

AVES; LEPUS; LEPUS AMERICANUS; MAMMALIA;

EID: 79551653609     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.1992     Document Type: Conference Paper

References (61)

1. Krebs, C. J., Boutin, S. & Boonstra, R. 2001 Ecosystem dynamics of the boreal forest: the Kluane project. New York, NY: Oxford University Press.
2. Batzli, G. O., White, R. G., Maclean, S. F., Pitelka, F. A. & Collier, B. D. 1980 The herbivore-based trophic system. In An arctic ecosystem (eds J. Brown, P. C. Miller, L. L. Tiezen & F. L. Bunnell), pp. 335-410, Stroudsburg, PA: Dowden, Hutchinson, and Ross.
3. Elton, C. S. 1924 Periodic fluctuations in the numbers of animals: their causes and effects. Br. J. Exp. Biol. 2, 119-163.
4. Chitty, D. & Elton, C. 1937 Canadian Arctic wild life enquiry, 1935-36. J. Anim. Ecol. 6, 368-385. (doi:10.2307/1193)
5. Chitty, D. 1960 Population processes in the vole and their relevance to general theory. Can. J. Zool. 38, 99-113. (doi:10.1139/z60-011)
6. Norrdahl, K. 1995 Population cycles in northern small mammals. Biol. Rev. 70, 621-637. (doi:10.1111/j.1469-185X.1995.tb01654.x)
7. Stenseth, N. C. 1999 Population cycles in voles and lemmings: density dependence and phase dependence in a stochastic world. Oikos 87, 427-461. (doi:10.2307/3546809)
8. Lambin, X., Krebs, C. J., Moss, R. & Yoccoz, N. G. 2002 Population cycles: inferences from experimental, modeling, and time series approaches. In Population cycles: the case for trophic interactions (ed. A. Berryman), pp. 155-176. New York, NY: Oxford University Press.
9. Korpimäki, E., Brown, P. R., Jacob, J. & Pech, R. P. 2004 The puzzles of population cycles and outbreaks of small mammals solved? Bioscience 54, 1071-1079. (doi:10. 1641/0006-3568 (2004) 054[1071:TPOPCA]2.0.CO;2)
10. Sheriff, M. J., Krebs, C. J. & Boonstra, R. 2010 The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk. Ecology 91, 2983-2994. (doi:10.1890/09-1108.1)
11. Oksanen, T., Oksanen, L., Dahlgren, J. & Olofsson, J. 2008 Arctic lemmings, Lemmus spp. and Dicrostonyx spp.: integrating ecological and evolutionary perspectives. Evol. Ecol. Res. 10, 415-434.
12. Klemola, T., Tanhuanpaa, M., Korpimäki, E. & Ruohomaki, K. 2002 Specialist and generalist natural enemies as an explanation for geographical gradients in population cycles of northern herbivores. Oikos 99, 83-94. (doi:10.1034/j.1600-0706.2002.990109.x)
13. Smith, M. J., White, A., Sherratt, J. A., Telfer, S., Begon, M. & Lambin, X. 2008 Disease effects on reproduction can cause population cycles in seasonal environments. J. Anim. Ecol. 77, 378-389. (doi:10.1111/j.1365-2656. 2007.01328.x)
14. Krebs, C. J., Lambin, X. & Wolff, J. O. 2007 Social behavior and self-regulation in murid rodents. In Rodent societies: an ecological and evolutionary perspective (eds J. O. Wolff & P. W. Sherman), pp. 173-181. Chicago, IL: University of Chicago Press.
15. Ginzburg, L. R. & Taneyhill, D. E. 1995 Higher growth rate implies shorter cycle, whatever the cause: a reply to Berryman. J. Anim. Ecol. 64, 294-295. (doi:10.2307/5764)
16. Turkington, R., John, E. & Dale, M. R. T. 2001 Herbs and grasses. In Ecosystem dynamics of the boreal forest (eds C. J. Krebs, S. Boutin & R. Boonstra), pp. 69-91. New York, NY: Oxford University Press.
17. Turkington, R., John, E., Watson, S. & Seccomb-Hett, P. 2002 The effects of fertilization and herbivory on the herbaceous vegetation of the boreal forest in north-western Canada: a 10-year study. J. Ecol. 90, 325-337. (doi:10. 1046/j.1365-2745.2001.00666.x)
18. Burn, C. R. & Zhang, Y. 2009 Permafrost and climate change at Herschel Island (Qikiqtaruk), Yukon Territory, Canada. J. Geophys. Res. 114, F02001. (doi:10.1029/2008JF001087)
19. Wilson, D., Krebs, C. J. & Sinclair, A. R. E. 1999 Limitation of collared lemming populations during a population cycle. Oikos 87, 382-398. (doi:10.2307/3546754)
20. Hodges, K. E., Krebs, C. J., Hik, D. S., Stefan, C. I., Gillis, E. A. & Doyle, C. E. 2001 Snowshoe hare demography. In Ecosystem dynamics of the boreal forest: the Kluane project (eds C. J. Krebs, S. Boutin & R. Boonstra), pp. 141-178. New York, NY: Oxford University Press.
21. Borchers, D. L. & Efford, M. G. 2008 Spatially explicit maximum likelihood methods for capture-recapture studies. Biometrics 64, 377-385. (doi:10.1111/j.1541-0420. 2007.00927.x)
22. Efford, M. G., Borchers, D. L. & Byrom, A. E. 2009 Density estimation by spatially explicit capture-recapture: likelihood-based methods. In Modeling demographic processes in marked populations (eds E. G. C. D. L. Thomson & M. J. Conroy), pp. 255-269. New York, NY: Springer.
23. Morris, D. W., Davidson, D. L. & Krebs, C. J. 2000 Measuring the ghost of competition: insights from density-dependent habitat selection on the coexistence and dynamics of lemmings. Evol. Ecol. Res. 2, 41-67.
24. Kausrud, K. L. et al. 2008 Linking climate change to lemming cycles. Nature 456, 93-97. (doi:10.1038/nature07442)
25. Gruyer, N., Gauthier, G. & Berteaux, D. 2010 Demography of two lemming species on Bylot Island, Nunavut, Canada. Polar Biol. 33, 725-736. (doi:10.1007/s00300-009-0746-7)
26. Chitty, H. 1950 Canadian Arctic wild life enquiry, 1943-1949: with a summary of results since 1933. J. Anim. Ecol. 19, 180-193. (doi:10.2307/1527)
27. Krebs, C. J., Kenney, A. J., Gilbert, S., Danell, K., Angerbjörn, A., Erlinge, S., Bromley, R. G., Shank, C. & Carriere, S. 2002 Synchrony in lemming and vole populations in the Canadian Arctic. Can. J. Zool. 80, 1323-1333. (doi:10.1139/z02-120)
28. Gilg, O., Sittler, B. & Hanski, I. 2009 Climate change and cyclic predator-prey population dynamics in the high Arctic. Global Change Biol. 15, 2634-2652. (doi:10.1111/j.1365-2486.2009.01927.x)
29. Reid, D. G., Krebs, C. J. & Kenney, A. J. 1997 Patterns of predation on noncyclic lemmings. Ecol. Monogr. 67, 89-108. (doi:10.1890/0012-9615 (1997) 067[0089: POPONL]2.0.CO;2)
30. Millar, J. S. 2001 On reproduction in lemmings. Ecoscience 8, 145-150.
31. Reid, D. G., Krebs, C. J. & Kenney, A. J. 1995 Limitation of collared lemming population growth at low densities by predation mortality. Oikos 73, 387-398. (doi:10. 2307/3545963)
32. Gilg, O., Hanski, I. & Sittler, B. 2003 Cyclic dynamics in a simple vertebrate predator-prey community. Science 302, 866-868. (doi:10.1126/science. 1087509)
33. Speakman, J. & Król, E. 2005 Limits to sustained energy intake IX: a review of hypotheses. J. Comp. Physiol. B 175, 375-394. (doi:10.1007/s00360-005-0013-3)
34. Mallory, F. F. & Brooks, R. J. 1978 Infanticide and other reproductive strategies in the collared lemming, Dicrostonyx groenlandicus. Nature 273, 144-146. (doi:10.1038/273144a0)
35. Millar, J. S. 2007 Nest mortality in small mammals. Ecoscience 14, 286-291. (doi:10.2980/1195-6860 (2007) 14[286:nmism]2.0.co;2).
36. Pitelka, F. A. 1957 Some characteristics of microtine cycles in the Arctic. In Arctic Biology pp. 73-88. Corvallis, Oregon: Oregon State College Biology Colloquium.
37. Schultz, A. M. 1964 The nutrient-recovery hypothesis for Arctic microtine cycles. II. Ecosystem variables in relation to the Arctic microtine cycles. In Grazing in terrestrial and marine environments (ed. D. J. Crisp), pp. 57-68. Oxford, UK: Blackwells.
38. Turchin, P. & Batzli, G. O. 2001 Availability of food and the population dynamics of arvicoline rodents. Ecology 82, 1521-1534. (doi:10.1890/0012-9658 (2001) 082 [1521:AOFATP]2.0.CO;2)
39. Gauthier, G., Berteaux, D., Krebs, C. J. & Reid, D. 2009 Arctic lemmings are not simply food limited-a comment. Evol. Ecol. Res. 11, 483-484.
40. Pitelka, F. A. & Batzli, G. O. 2007 Population cycles of lemmings near Barrow, Alaska: a historical review. Acta Theriol. 52, 323-336.
41. Ims, R. A., Henden, J.-A. & Killengreen, S. T. 2008 Collapsing population cycles. Trends Ecol. Evol. 23, 79-86. (doi:10.1016/j.tree.2007.10. 010)
42. Elton, C. & Nicholson, M. 1942 The ten-year cycle in numbers of the lynx in Canada. J. Anim. Ecol. 11, 215-244. (doi:10.2307/1358)
43. Keith, L. B. 1981 Population dynamics of hares. In Proceedings of the World Lagomorph Conference (eds K. Myers & C. D. MacInnes), pp. 395-440. Guelph, Ontario: University of Guelph.
44. Krebs, C. J., Boutin, S. & Gilbert, B. S. 1986 A natural feeding experiment on a declining snowshoe hare population. Oecologia 70, 194-197. (doi:10.1007/BF00379239)
45. Boutin, S., Krebs, C. J., Boonstra, R., Sinclair, A. R. E. & Hodges, K. E. 2002 Understanding the snowshoe hare cycle through large-scale field experiments. In Population cycles: the case for trophic interactions (ed. A. Berryman), pp. 69-91. New York, NY: Oxford University Press.
46. Krebs, C. J., Boutin, S., Boonstra, R., Sinclair, A. R. E., Smith, J. N. M., Dale, M. R. T., Martin, K. & Turkington, R. 1995 Impact of food and predation on the snowshoe hare cycle. Science 269, 1112-1115. (doi:10.1126/science.269.5227.1112)
47. Cary, J. R. & Keth, L. B. 1979 Reproductive changes in the 10-year cycle of snowshoe hares. Can. J. Zool. 57, 375-390.
48. Boonstra, R., Hik, D., Singleton, G. R. & Tinnikov, A. 1998 The impact of predator-induced stress on the snowshoe hare cycle. Ecol. Monogr. 68, 371-394. (doi:10. 1890/0012-9615 (1998) 068[0371:TIOPIS]2.0.CO;2)
49. Sheriff, M. J., Krebs, C. J. & Boonstra, R. 2009 The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J. Anim. Ecol. 78, 1249-1258. (doi:10.1111/j.1365-2656.2009.01552.x)
50. O'Donoghue, M., Boutin, S., Krebs, C. J. & Hofer, E. J. 1997 Numerical responses of coyotes and lynx to the snowshoe hare cycle. Oikos 80, 150-162. (doi:10.2307/3546526)
51. Smith, J. N. M., Krebs, C. J., Sinclair, A. R. E. & Boonstra, R. 1988 Population biology of snowshoe hares II. Interactions with winter food plants. J. Anim. Ecol. 57, 269-286. (doi:10.2307/4778)
52. Murray, D. L. & Boutin, S. 1991 The influence of snow on lynx and coyote movements in southwestern Yukon: does morphology affect behaviour? Oecologia 88, 463-469.
53. O'Donoghue, M., Boutin, S., Krebs, C. J., Zuleta, G., Murray, D. L. & Hofer, E. J. 1998 Functional responses of coyotes and lynx to the snowshoe hare cycle. Ecology 79, 1193-1208. (doi:10.2307/176736)
54. Stenseth, N. C., Shabbar, A., Chan, K.-S., Boutin, S., Rueness, E. K., Ehrich, D., Hurrell, J. W., Lingjærde, O. C. & Jakobsen, K. S. 2004 Snow conditions may create an invisible barrier for lynx. Proc. Natl Acad. Sci. USA 101, 10632-10634. (doi:10.1073/pnas.0308674101)
55. Stenseth, N. C. et al. 2004 The effect of climatic forcing on population synchrony and genetic structuring of the Canadian lynx. Proc. Natl Acad. Sci. USA 101, 6056-6061. (doi:10.1073/pnas.0307123101)
56. Mowat, G., Poole, K. G. & O'Donoghue, M. 2000 Ecology of lynx in northern Canada and Alaska. In Ecology and conservation of lynx in the United States (eds L. F. Ruggiero, K. B. Aubry, S. W. Buskirk, G. M. Koehler, C. J. Krebs, K. S. McKelvey & J. R. Squires), pp. 265-306. Denver, CO: University Press of Colorado.
57. Poole, K. G. & Graf, R. P. 1996 Winter diet of marten during a snowshoe hare decline. Can. J. Zool. 74, 456-466. (doi:10.1139/z96-053)
58. Sibly, R. M. & Hone, J. 2002 Population growth rate and its determinants: an overview. Phil. Trans. R. Soc. Lond. B 357, 1153-1170. (doi:10.1098/rstb.2002.1117)
59. Lindenmayer, D. B. & Likens, G. E. 2009 Adaptive monitoring: a new paradigm for long-term research and monitoring. Trends Ecol. Evol. 24, 482-486. (doi:10. 1016/j.tree.2009.03.005)
60. Graham, I. M. & Lambin, X. 2002 The impact of weasel predation on cyclic field-vole survival: the specialist predator hypothesis contradicted. J. Anim. Ecol. 71, 946-956. (doi:10.1046/j.1365-2656.2002. 00657.x)
61. Korpimäki, E., Klemola, T., Norrdahl, K., Oksanen, L., Oksanen, T., Banks, P. B., Batzli, G. O. & Henttonen, H. 2003 Vole cycles and predation. Trends Ecol. Evol. 18, 494-495. (doi:10.1016/S0169-5347 (03) 00159-9)