Population cycles in small mammals: The problem of explaining the low phase

Ecology

Volumn 79, Issue 5, 1998, Pages 1479-1488

  Boonstra, Rudy ^a   Krebs, Charles J ^b   Stenseth, Nils Chr ^c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Extrinsic mechanisms; Intrinsic mechanisms; Lemmus spp.; Lepus americanus; Low phase; Microtines; Microtus spp.; Population cycles; Population regulation; Snowshoe hares

Indexed keywords

CYCLICITY; MAMMAL; POPULATION DYNAMICS;

EID: 0031857698     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/0012-9658(1998)079[1479:PCISMT]2.0.CO;2     Document Type: Article

References (100)

1. Agrell, J., S. Erlinge. J Nelson. C Nilsson. and l Persson 1995. Delayed density dependence in a small-rodent population. Proceedings of the Royal Society of London. Series B 262:65-70.
2. Andersson, M., and S. Jonasson. 1986. Rodent cycles in relation to food resources on an alpine heath. Oikos 46: 93-106.
3. Bergeron, J.-M., and J Jodoin. 1993. Intense grazing by voles (Microtux peiinxylvunicux) and its effect on habitat quality. Canadian Journal of Zoology 71:1823-1830.
4. Bondrup-Nielsen, S., and R. A. Ims. 1988. Demography during a population crash of the wood lemming. Myopus schisticolor. Canadian Journal of Zoology 66:2442-2448.
5. Boonslra, R. 1985. Demography of Microlus pennxylvanicux in Southern Ontario: enumeration versus Jolly Seher estimation compared. Canadian Journal of Zoology 63:1174-1180.
6. _ 1994. Population cycles in microtines: the senescence hypothesis. Evolutionary Ecology 8:196-219.
7. Boonstra, R., and P. T. Boag. 1987. A test of the Chilly hypothesis: inheritance of life history traits in meadow voles Microtus pennsylvanicus. Evolution 41:929-947.
8. Boonstra, R., D. Hik, G. R. Singleton, and A. Tinnikov. 1998. The impact of predator-induced stress on the snowshoe hare cycle. Ecological Monographs 68. in press.
9. Boonstra, R., and W. M. Hochachka. 1997. Maternal effects and additive genetic inheritance in the collared lemming (Dicroxtonvx groenlandicus). Evolutionary Ecology 11: 169-182.
10. Boonstra, R., W. M Hochachka, and I., Pavone. 1994. Helerozygosity, aggression, and population fluctuations in meadow voles (Microlus pennsvlvanicus). Evolution 48: 1350-1363.
11. Boonstra, R., and G. R. Singleton. 1993. Population declines in the snowshoe hare and the role of stress. General and Comparative Endocrinology 91:126-143.
12. Boutin, S. 1984. Effect of late winter food addition on numbers and movements of snowshoe hares. Oecologia 62:393400.
13. Bryant, J P., G. D. Wicland, T. Clausen, and P. Kuropat. 1985. Interactions ot snowshoe hare and feltleaf willow in Alaska. Ecology 66:1564-1573.
14. Charnov, E. L., and J. P. Finerty. 1980. Vole population cycles: a case for kin selection? Oecologia 45:1-2.
15. Chcrnyavskii, F. B. 1979. Population dynamics and population indices of Lenimus sihiricus and Dicrtstonyx torquatus on Wrangel Island. Zoologichcskii zhurnal 58:553-563.
16. Chernyavskii, E B., and V. I. Doroggoi. 1981. O roli khishchnikov v dinamike chislennosti lemmingov (na primere Ostrava Vrangelya.) [On the role of predators in the dynamics of lemming numbers (an example from Wrangel Island)]. Pages 32-50 in V. I., Kontrimavichus, editor. Ekologiya mlekopitayushchikh severo-vostochnoi Sibiri. I Ecology of mammals of northeast Siberia.] (In Russian.) Izdatelstvo Nauka, Moskva, Russia.
17. Chilly, D. 1967. The natural selection of self-regulatory behaviour in animal populations. Proceedings of the Ecological Society of Australia 2:51-78.
18. Deseotcaux, J.-P., and S. Mihok. 1986. Serologie study on the prevalence of murine viruses in a population of wild meadow voles (Microtus pennsvlvanicus). Journal of Wildlife Diseases 22:314-319.
19. Desy, E. A., and G. O. Batzli. 1989. Effects of food availability and predation on prairie vole demography: a field experiment. Ecology 70:41 1-421.
20. Fitzgerald, B. M. 1977. Weasel predation on a cyclic population of the montane vole (Micrams inontanus) in California. Journal of Animal Ecology 46:367-397.
21. Framstad, E., N. C. Stenseth, O N. Bjørnstad. and W, Halck. 1997. Limit cycles in Norwegian lemmings: tensions between phase-dependence and density-dependence. Proceedings of the Royal Society of London, Section B. 264: 31-38.
22. Framstad, E., N. C. Stenseth, and E., Østbye. 1993. Time series analysis of population fluctuations of Lemmus lemmus. Pages 97-115 in N. C. Slenseth and R. A. Ims, editors. The biology of lemmings. Academic Press, London, UK.
23. Fredga, K., R. Fredriksson, S. Bondrup-Niclsen, and R. A. Ims. 1993. Sex ratio, chromosomes, and isozyines in natural populations of the wood lemming (Myopus schisticoIor). Pages 465-491 in N. C. Stenseth and R. A. Ims, editors. The biology of lemmings. Academic Press, London, UK.
24. Fuller, C. A., and A. R. Blaustein. 1996. Effects of the parasite Kimeria ariymensis on survival of deer mice (Pentmyscus maniculatus). Ecology 77:2196-2202.
25. Gaines, M. S. 1985. Genetics. Pages 845-883 in R H. Tamarin, editor. Biology of New World Microtus. American Society of Mammalogists. Special Publication Number 8.
26. Grodzinski, J. 1977. Connections between predatory birds and mammals and their prey. Acta Theriologica 22:399430.
27. Hanski, I., and H. Henttonen. 1996. Predation on competing rodent species: a simple explanation of complex patterns. Journal of Animal Ecology 65:220-232.
28. Hanski, I., and F., Korpimäki. 1995. Microtine rodent dynamics in northern Europe: parameterizcd models for the predator-prey interaction. Ecology 76:840-850.
29. Hanski, I., P Turchin, E. Korpimäki. and H. Henttonen. 1993. Population oscillations of boreal rodents: regulation by mustclid predators leads to chaos. Nature 364:232-235.
30. Hansson, L. 1987. An interpretation of rodent dynamics as due to trophic interactions. Oikos 50:308-318.
31. Haukioja, E., K. Kapiainen, P Niemelä, and J. Tuomi. 1983. Plant availability hypothesis and other explanations of herbivore cycles: complementary or exclusive alternatives. Oikos 40:419-432.
32. Haukisalmi, V., H. Henttonen, and F. Tenora. 1988. Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57:807-825.
33. Heikkilä. J., A. Below, and I. Hanski. 1994. Synchronous dynamics of microtine rodent populations on islands in Lake Inari in northern Fennoscandia: evidence for regulation by mustelid predators. Oikos 70:245-252.
34. Hemtonen, H. 1987. The impact of spacing behavior in microtine rodents on ihe dynamics of least weasels Mustela nivalis: a hypothesis. Oikos 50:366-370.
35. Henttonen, H., T. Oksanen, A. Jorukka, and V. Haukisalmi. 1987 Him much do weasels shape microtine cycles in the northern Fennoscandian taiga.' Oikos 50:353-365.
36. Hik, D. S. 1995. Does risk ot predation influence population dynamics?Evidence Irom the cyclic decline of snowshoe hares Wildlife Research 22:115-129.
37. Ḧornfeldt. B. 1978. Synchronous population fluctuations in voles, small game, owls. and tulaemia in northern Sweden Oecologia 32:141-152.
38. _ 1994. Delayed density dependence as a determinant of vole cycles. Ecology 75. 791-806.
39. Ishihashi, Y., T. Saitoh. S. Abe. and M C. Voshula 1997 Sex-related spatial kin structure in a spring population of grey-sided voles Clethrionomys rufocuanus as revealed by mitochondrial and microsatellite DNA analyses. Molecular Ecology 6:63-71.
40. Kaitala. V., T. Mappes, and H. Ylönen. 1997. Delayed female reproduction in equilibrium and chaotic populations. Evolutionary Ecology 11:105-126.
41. Kawata, M. 1990. Fluctuating populations and kin interaction in mammals. Trends in Ecology and Evolution 5:1720.
42. Keith, I. M., L. B. Keith, and C. R. Cary. 1986. Parasitism in a declining population of snowshoe hares. Journal of Wildlife Diseases 22:349-363.
43. Keith, L., B. 1990 Dynamics of snowshoe hare populations. Current Mammalogy 2:119-195.
44. Keith, L. B., C. R. Cary, O. J. Rongstad, and M. C Brittingham. 1984. Demography and ecology of a declining snowshoe hare population. Wildlife Monographs 90:1-43.
45. Keith, I. B., C. R. Cary, T. M. Yuill, and I. M. Keith. 1985. Prevalence of helminths in a cyclic snowshoe hare population. Journal of Wildlife Diseases 21:233-253.
46. Keith, L. B., A. W. Todd, C. J. Brand, R. S. Adamcik. and D. H. Rusch. 1977. An analysis of predation during a cyclic fluctuation of snowshoe hares. Proceedings of the International Congress of Game Biologists 13:151-175.
47. Keith, L. B., and L. A. Windberg. 1978. A demographicanalysis of the snowshoe hare cycle. Wildlife Monographs 58:1-70.
48. Kirkpatrick, M., and R. Lande. 1989. The evolution of maternal characters. Evolution 43:485-503.
49. Klemola, T., M. Koivula, E. Korpim̈ki. and K. Norrdahl. 1997a. Size of internal organs and forage quality between cycle phases in Microtus voles. Oikos 80:61-66.
50. Klemola. T. M. Koivula, E. Korpim̈ki. and K. Norrdahl. 1997b. Small muslelid predation slows population growth of Microtus voles: a prcdalor reduction experiment. Journal of Animal Ecology 66:607-614.
51. Kokko, H., and E. Rama 1996. Evolutionary optimality of delayed breeding in voles. Oikos 77:173-175.
52. Korpim̈ki, E., and C. J Krebs. 1996. Predation and population cycles in small mammals Bio Science 46:754-764.
53. Korpim̈ki, E., and K. Norrdahl. 1991. Numerical and functional responses of Kestrels. Short-eared Owls, and Longeared Owls to vole densities. Ecology 72:814-826.
54. Korpim̈ki. E., K. Norrdahl, and T. Rinta-Jarkasi. 1991. Responses of stoats and least weasels to fluctuating food abundances: is the low phase of the vole cycle due to muslelid predation? Oecologia 88:552-561.
55. Korpim̈ki. E., K. Norrdahl. and J. Valkama. 1994. Reproductive investment under fluctuating predation risk: microtine rodents and small mustelids. Evolutionary Ecology 8:357-368.
56. Krebs, C J. 1996. Population cycles revisited. Journal of Mammalogy 77:8-24.
57. Krebs. C. J., R. Boonstra. and A. J. Kenney. 1995a. Population dynamics of the collared lemming and the tundra vole ai Pearce Poinl. Northwest Territories, Canada. Oecologia 103:481-489.
58. Krebs, C. J., S. Boutin. R. Boonstra. A. R. F., Sinclair. J. N M. Smith, M. R. T. Dale, K. Martin, and R. Turkinglon 1995b. Impact of food and predation on the .snowshoe hare cycle. Science 269:1 112-1115.
59. Krehs. C J., B. S. Gilbert, S. A. Boulin. A. R. E. Sinclair, and J. N. M. Smith. 1986. Population hiology of .snowshoe hares. I. Demography of food-supplemented populations in the southern Yukon. 1976-1984 Journal of Animal Ecology 55.963-982.
60. Krebs. C. J., and J. H. Myers. 1974. Population cycles in Mtiall mammals Advance in Ecological Research 8:267399.
61. l.aakkonen, J. 1996 Characlen/ation and ecologs of Pnue inocystis carnii infection in wild small mammals. Dissertation. University of Helsinki. Helsinki. Finland.
62. Laine. K., and H Henltonen. 1983. The role of plant production in microtine csclcs in northern hennoscandia. Oikos 40:407-4 18.
63. Lambin, X., R. A Ims. H. Sleen, and N. G Yocxco/. 1995. Vole cycles. Trends in Ecology and Evolution 10:204.
64. Lambin, X., and C.J. Krebs 1991. Can changes in female relatedness influence microtine dynamics? Oikos 61:126-132.
65. Lindroth, K. L., and G. O. Batzli. 1986. Inducible plant chemical defences: a cause of vole population cycles? Journal of Animal Ecology 55:431-450.
66. Marcström V., R. E. Kenward, and E. Engren. 1988. The impact of predation on boreal tetraonids during vole cycles: an experimental study. Journal of Animal Ecology 57:859-872.
67. Maynard Smith, J., and N. C. Stenseth. 1978. On the evolutionary stability of the female-biased sex ratio in the wood lemming (Myopus schisticolor): the effect of inbreeding. Heredity 41:205-214
68. McRoberts, R. E., I., D. Mech. and R. O. Pcterson. 1995. The cumulative effect of consecutive winters' snow depth on moose and deer populations: a defence Journal of Animal Ecology 64:131-135.
69. Mihok. S., and R. Boonstra. 1992. Breeding performance in captivity of meadow voles (Micnilus pennsylvanicus) from decline- and increase-phase populations. Canadian Journal of Zoology 70:1561-1566.
70. Mihok, S., T. Law ton, and B. Schwarti., 1988. Fates and movements of meadow voles (Mirrnlus pennsylvanicus) following a population decline. Canadian Journal of Zoology 66:323-328.
71. Mihok. S., B. N. Turner, and S. I., Iverson. 1985. The characterization of vole population dynamics. Ecological Monographs 55:399-420.
72. Moss. R., W. Watson, and R. Parr. 1996. Experimental prevention of a population cycle in Red Grouse Ecology 77: 1512-1530.
73. Mountford, M. D., W. Watson, R. Moss, R. Parr, and P. Rothery. 1990. Land inheritance and population cycles of Red Grouse. Pages 78-83 in A. N. Lance and J. N. Lawton. editors Red Grouse population processes. Royal Society for the Protection of Birds, Sandy, Bedfordshire. UK.
74. Norrdahl, K. 1995. Population cycles in northern small mammals. Biological Reviews 70:621-637.
75. Norrdahl. K., and E. Korpim̈ki. 1995 Mortality factors in a cyclic vole population. Proceedings of the Royal Society of London, Series B 261:49-53.
76. Oksanen. I., T. Oksanen, A. Lukkari, and S. Siren, 1987. The role of phenol-based induciblc defense in the interaction between tundra populations of the vole Clethrionomys rufocanus and the dwarf shrub Vaccinium mvrtillus. Oikos 50:371-380.
77. Ostfeld, R. S. 1992a. Small herbivores in a patchy environment: individual strategies and population responses. Pages 43-74 in M. D. Hunter, T. Ohgushi, and P. W. Price, editors. Effects of resource distribution on animal-plant interactions. Academic Press, New York, New York, USA.
78. _ 1992b. Do changes in female relatedness determine demographic patterns in microtine rodents? Oikos 65:531534.
79. Ostfeld, R. S., C. D. Canham, and S. R. Pugh. 1993. Intrinsic density-dependent regulation of vole populations. Nature 366:259-261.
80. Pearson, O. P. 1966. The prey of carnivores during one cycle of mouse abundance Journal of Animal Ecology 35:217233.
81. Pugh. S., and R. H. Tamarin. 1990. A test of the Charnov and Finerty hypothesis of population regulation in meadow voloes. Pages 111-120 in R. H. Tamarin. R S. Ositfeld. S. R Pugh. and G. Bujalska. editors. Social systems and populalion cycles in voles. Birkhauser Verlag. Basel. Switzerland.
82. Reid. D G., C. J. Krebs, and A. J. Kenney. 1995. Limitation of collared lemming population growth at low densities by predation mortality. Oikos 73:387-398.
83. Rossiter. M. C. 1991 Environmentally based maternal effects: a hidden force in insect population dynamics? Oecologia 87:288-294.
84. _ 1994. Maternal effects hypothesis of herbivore outbreak: a framework for the inclusion of population-quality variables as central features of herbivore population-dynamics models. BioSciencc 44:752-763.
85. Sapolsky, R. 1992. Stress, the aging brain, and the mechanisms of neuronal death MIT Press. Cambridge. Massachusetts. USA.
86. _ 1996. Why stress is bad for your brain. Science 273: 749-750.
87. Seldal, T., K.-J Andersen, and C. Hogsledt. 1994. Grazinginduced protcinase inhibitors: a possible cause for lemming population cycles. Oikos 70:3-11.
88. Sinelair, A. R. E., C. J. Krebs, J. N. M. Smith. and S. Boulin. 1988. Population biology of snowshoe hares. III. Nutrition, plant secondary compounds, and food limitation. Journal of' Animal Ecology 57.787-806.
89. Sittler, B. 1995. Response of stoats (Mustela erminea) to a fluctuating lemming (Dicrostonyx groenlandicus) population in northeast Greenland: preliminary results from a long-term study. Annales Zoologici Fennici 32:79-92.
90. Smith, J. N M., C. J. Krebs. A. R. E. Sinclair, and R. Boonstra. 1988. Population biology of snowshoe hares. II. Interactions with winter food plants. Journal of Animal Ecology 57:269-286.
91. Smith, M. H., C. T. Garten, and P. R. Ramscy. 1975 Genie heterozygosity and population dynamics in small mammals. Pages 85-102 in C. L. Markert, editor. Isozymes IV. Genetics and evolution. Academic Press, New York, New York, USA.
92. Sonerud, G. A. 1988. What causes extended lows in microtine cycles? Oecologia 76:37-42.
93. Stenseth. N. C., O. N. Bjornstad. and W. Falck. 1996. Is spacing behaviour coupled with predation causing the microtinc density cycle? A synthesis of current process-oriented and pattern-oricnfed studies. Proceedings of the Royal Society of London. Series B 263:1423-1435.
94. Stenseth, N. C., and R. A. Ims. 1993 Population dynamics of lemmings: temporal and spatial variation: an introduction Pages 61-96 in N. C. Stenseth and R. A. Ims, editors The biology of lemmings. Academic Press, London, UK.
95. Stenseth, N. C., and W. Z. Lidicker, Jr. 1992. Prcsaturation and saturation dispersal 15 years later: some theoretical considerations. Pages 201-223 in N. C. Stenseth and W. Z. Lidicker, Jr., editors. Animal dispersal. Chapman and Hall, London, UK
96. Stenseth, N. C., and A. Lomnicki. 1990. On the CharnovHinerty hypothesis: the unproblemalic transition from docile to aggressive and the problematic transition from aggressive to docile. Oikos 58:234-238.
97. Taitt, M J., and C. J. Krebs. 1981. The effect of extra food on small-rodent populations. II. Voles (Microtus townsendii). Journal of Animal Kcology 50:125-137.
98. Tkadlcc, E., and J. Zejda. 1998. Small rodent fluctuations: the effects of age structure and seasonality. Evolutionary Ecology 12:191-210.
99. Weir, B S. 1996. Genetic data analysis II. Sinauer Associates. Sunderland. Massachusetts, USA.
100. Ylonen, H. 1994. Vole cycles and antiprcdatory behaviour. Trends in Ecology and Evolution 9:426-430.