Cycles of voles, predators, and alternative prey in boreal Sweden

Abstract: Bank voles, grey-sided voles, and field voles had synchronous 3-4 year density cycles with variable amplitudes which averaged about 200-fold in each species. Cycles of vole predators (red fox and Tengmalm's owl), and their (foxes') alternative prey (mountain hare and forest grouse) lagged behind the vole cycles.The nomadic Tengmalm's owl responded with a very rapid and strong numerical increase to the initial cyclic summer increase of voles (the owl’s staple food). Owl breeding densities in the springs were highly correlated with vole supply in the previous autumns. This suggested that the number of breeding owls was largely determined in the autumn at the time of the owl's nomadic migrations, and that immigration was crucial for the rapid rise in owl numbers. The owl's numerical response was reinforced by the laying of earlier and larger clutches when food was plentiful. In addition, the owl has an early maturation at one year of age.The transition between subsequent vole cycles was characterized by a distinct shift in rate of change in numbers from low to high or markedly higher values in both summer and winter. Regulation increased progressively throughout the cycle since the rate of change decreased continuously in the summers. Moreover, there was a similar decrease of the rate of change in winter. Rate of change was delayed density-dependent. The delayed density-dependence had an 8 month time-lag in the summers and a 4 month time-lag in the winters relative to the density in previous autumns and springs, respectively. These findings suggest that vole cycles are likely to be generated by a time-lag mechanism. On theoretical grounds, it has been found that a delayed density- dependence of population growth rate with a 9 month time-lag caused stable limit cycles with a period between 3 and 4 years. Some mechanisms for the delayed density-dependence are suggested and discussed. The mechanisms are assumed to be related to remaining effects of vole populations past interactions with predators, food supplies, and/or diseases.Unlike the other voles, the bank vole had regular and distinct seasonal declines in density over winter. These declines are proposed to be due to predation, mainly by Tengmalm's owl. Supranivean foraging for epiphytic tree lichens and conifer seeds most likely explains why this species was frequently taken by the owl under snow-rich conditions.The alternative prey hypothesis predicts that a reduction of predator numbers should increase the number of alternative prey. Alternative prey should be less effectively synchronized to the vole cycle by predation at declining and low vole (main prey) densities; they may also lose their 3-4 year cyclicity. The appearance of sarcoptic mange among foxes in northern Sweden in the mid 1970s provided an opportunity to "test" these ideas, and these were found to be supported. In areas with highest mange infection rates, foxes declined markedly from the late 1970s to mid 1980s, whereas hare numbers rose rapidly and appeared non-cyclic.