Erkki Korpimäki

SMALL‐RODENT DYNAMICS AND PREDATION

The hypothesis that the regular multiannual population oscillations of boreal and arctic small rodents (voles and lemmings) are driven by predation is as old as the scientific study of rodent cycles itself. Subsequently, for several decades, the predation hypothesis fell into disrepute, possibly because the views about predation and rodent dy- namics were too simplistic. Here we review the work that has been done on the predation hypothesis primarily in Fennoscandia over the past decade. Models of predator-prey interaction have been constructed for the least weasel (Mustela nivalis) and the field vole (Microtus agrestis), which are considered to be the key specialist predator and the key prey species in the multispecies communities in the boreal forest region in Fennoscandia. The basic model has been parameterized with independent field data, and it predicts well the main features of the observed dynamics. An extension of the model also including generalist and nomadic avian predators predicts correctly the well- documented and striking geographic gradient in rodent oscillations in Fennoscandia, with the amplitude and cycle period decreasing from north to south. These geographic changes are attributed to the observed latitudinal change in the density of generalist and nomadic predators, which are expected to have a stabilizing effect on rodent dynamics. We review the other observational, modeling, and experimental results bearing on the predation hypothesis and conclude that it accounts well for the broad patterns in rodent oscillations in Fennoscandia. We discuss the application of the predation hypothesis to other regions in the northern hemisphere. The predation hypothesis does not make predictions about multiannual and latitudinal changes in body size, behavior, and demography of ro- dents, which may have some population-dynamic consequences. With the current evidence, however, we consider it unlikely that the phenotypic and genotypic composition of pop- ulations would be instrumental for generating the broad patterns in rodent oscillations.

Alien predators are more dangerous than native predators to prey populations

Alien predators are widely considered to be more harmful to prey populations than native predators. To evaluate this expectation, we conducted a meta-analysis of the responses of vertebrate prey in 45 replicated and 35 unreplicated field experiments in which the population densities of mammalian and avian predators had been manipulated. Our results showed that predator origin (native versus alien) had a highly significant effect on prey responses, with alien predators having an impact double that of native predators. Also the interaction between location (mainland versus island) and predator origin was significant, revealing the strongest effects with alien predators in mainland areas. Although both these results were mainly influenced by the huge impact of alien predators on the Australian mainland compared with their impact elsewhere, the results demonstrate that introduced predators can impose more intense suppression on remnant populations of native species and hold them further from their predator-free densities than do native predators preying upon coexisting prey.

NUMERICAL AND FUNCTIONAL RESPONSES OF KESTRELS, SHORT-EARED OWLS, AND LONG-EARED OWLS TO VOLE DENSITIES'

We studied numerical and functional responses of breeding European Kes- trels (EK) (Falco tinnunculus), Short-eared Owls (SO) (Asio flammeus), and Long-eared Owls (LO) (Asio otus) during 1977-1987 in 47 km2 of farmland in western Finland. The pooled mean yearly breeding density varied from 0.1 to 2.4 pairs/km2. The number of nesting EKs (range 2-46 pairs), SOs (0-49), and LOs (0-19) fluctuated in close accordance with the spring density of Microtus (M. agrestis and M. epiroticus) voles. The mean yearly number of fledglings produced per pair ranged from 0.4 to 3.8 and, for each species, was positively correlated with spring density of Microtus voles. Due to their high degree of mobility, EKs, SOs, and LOs were able to track the population fluctuations of their mi- crotine prey without time lags. An increase in microtine densities caused a rapid immi- gration into the study area and a decrease caused a rapid emigration from the area. Microtus voles were the most important prey group by mass in the diet of each species. Water voles, bank voles, shrews, and small birds were the most frequent alternate prey. The spring density of Microtus spp. was positively correlated with the percentage of these voles in the diet of EK, SO, and LO. The pooled functional response curve of these three raptor species to the fluctuating densities of Microtus spp. was close to linear, indicating that consumption rates are independent of vole densities. Breeding EKs, SOs, and LOs seemed to take a larger proportion of voles available in peak years than in low ones.

Predation and Population Cycles of Small Mammals A reassessment of the predation hypothesis

The periodicity of mass occurrence of some northern small rodents has been known from at least the mid-sixteenth century, when Archbishop of Uppsala, Sweden, Olaus Magnus, published two reports on the phenomenon. He suggested that lemming abundances peaked at intervals of approximately three years (Stenseth and Ims 1993a). Elton (1942) initiated research on periodic fluctuations in small mammal populations, and since then such fluctuations have been the focus of much research and controversy in animal ecology. Cyclic fluctuations of population densities of many northern mammals are characterized by a regular period (the interval between successive density peaks) and a highly variable amplitude (the ratio of maximum to minimum population density). In the boreal zone of North America and some parts of Siberia, the cycle period is usually 9-10 (811) years, and the cycle amplitude

Responses of stoats and least weasels to fluctuating food abundances: is the low phase of the vole cycle due to mustelid predation?

SummaryWe studied responses of stoats and least weasels to fluctuating vole abundances during seven winters in western Finland. Density indices of mustelids were derived from snow-tracking, diet composition from scat samples, and vole abundances from snap-trapping. Predation rate was estimated by the ratio of voles to mustelids and by the vole kill rate by predators (density of predator x percentage of voles in the diet). We tested the following four predictions of the hypothesis that small mustelids cause the low phase of the microtine cycle. (1) The densities of predators should lag well behind the prey abundances, as time lags tend to have destabilizing effects. The densities of stoats fluctuated in accordance with the vole abundances, whereas the spring densities of least weasels tracked the vole abundances with a half-year lag and the autumn densities with a 1-year lag. (2) Predators should not shift to alternative prey with declining vole densities. The yearly proportion of Microtus voles (the staple prey) in the diet of stoats varied widely (range 16–82%) and was positively correlated with the winter abundance of these voles. In contrast, the same proportion in the food of least weasels was independent of the vole abundance. (3) The ratio of voles to small mustelids should be smallest in poor vole years and largest in good ones. This was also observed. (4) Vole densities from autumn to spring should decrease more in those winters when vole kill rates are high than when they are low. The data on least weasels agreed with this prediction. Our results from least weasels were consistent with the predictions of the hypothesis, but stoats behaved like “semi-generalist” predators. Accordingly, declines and lows in the microtine cycle may be due to least weasel predation, but other extrinsic factors may also contribute to crashes.

EXPERIMENTAL REDUCTION OF PREDATORS REVERSES THE CRASH PHASE OF SMALL‐RODENT CYCLES

The mechanisms driving short-term (3–5 yr) cyclic fluctuations in densities of boreal small rodents, and especially, those causing a crash in numbers, have remained a puzzle, although food shortage and predation have been proposed as the main factors causing these fluctuations. In the first large-scale vertebrate predator manipulation experiment with sufficient replication, densities of small mustelids (the least weasel Mustela nivalis and the stoat M. erminea) and avian predators (mainly the Eurasian Kestrel Falco tinnunculus and Tengmalm’s Owl Aegolius funereus) were reduced in six different areas, 2–3 km2 each, in two crash phases (1992 and 1995) of the 3-yr cycle of voles (field vole Microtus agrestis, sibling vole M. rossiaemeridionalis, and bank vole Clethrionomys glareolus). The reduction of all main predators reversed the decline in density of small rodents in the subsequent summer, whereas in areas with least weasel reduction and in control areas without predator manipulation, small rodent densit...

DOES MOBILITY OR SEX OF VOLES AFFECT RISK OF PREDATION BY MAMMALIAN PREDATORS

Animals gain fitness benefits if they can increase their survival prospects by reducing mobility under temporarily high predation risk. We used miniature radio collars to determine whether mobility affects the risk of predation on breeding field voles (Microtus agrestis) and sibling voles (M. rossiaemeridionalis) by their main predators, small carni- vores, in a population with cyclically fluctuating numbers and predation risk. There was a significant association of mobility with predation risk: voles killed by small carnivores moved more than did voles that survived. An experimental reduction of predation risk significantly affected vole mobility: voles moved more under reduced predation risk. Sex, season, and phase of the vole cycle explained a similar or larger proportion of the observed variation in the number of killed voles than did mobility. Carnivores killed more female than male voles, predation risk was higher in the decline phase than in the increase phase of the cycle, and predation risk was also higher in spring than in early summer. However, voles cannot change sex, season, or the phase of their cycle, whereas they can alter their mobility. These results offer novel observational and experimental support for the hypoth- esis that animals may increase their survival prospects by reducing mobility. The female- biased prey choice of small carnivores implies that they have a stronger impact on prey population dynamics than avian predators, which have previously been shown to kill more males than females.

Dynamic effects of predators on cyclic voles: field experimentation and model extrapolation

Mechanisms generating the well-known 3–5 year cyclic fluctuations in densities of northern small rodents (voles and lemmings) have remained an ecological puzzle for decades. The hypothesis that these fluctuations are caused by delayed density–dependent impacts of predators was tested by replicated field experimentation in western Finland. We reduced densities of all main mammalian and avian predators through a 3 year vole cycle and compared vole abundances between four reduction and four control areas (each 2.5–3 km2). The reduction of predator densities increased the autumn density of voles fourfold in the low phase, accelerated the increase twofold, increased the autumn density of voles twofold in the peak phase, and retarded the initiation of decline of the vole cycle. Extrapolating these experimental results to their expected long–term dynamic effects through a demographic model produces changes from regular multiannual cycles to annual fluctuations with declining densities of specialist predators. This supports the findings of the field experiment and is in agreement with the predation hypothesis. We conclude that predators may indeed generate the cyclic population fluctuations of voles observed in northern Europe.

Predation of Tengmalm's owls: numerical responses, functional responses and dampening impact on population fluctuations of microtines

The predation of Tengmalms owls in the breeding season was studied during 1977-87 in western Finland. The yearly number of breeding pairs (range 1-26) and nonbreeding males (0-10) in the study area (100 km2) was positively related to the number of available Microtus (M. agrestis and M. epiroticus) and Clethrionomys glareolus. The mean number of fledglings produced per pair was also positively correlated with the numbers of voles. The owls were able to track without time lags the population fluctuations of their microtine prey due to the high degree of mobility, vole-supply-dependent adult and juvenile survival, large reproductive potential and early maturity. The density of Microtus voles was the most important factor determining the diet composition of breeding owls. The functional response curve to the changing numbers of Microtus spp. was very close to linear and did not level off at the high vole densities. This indicated a constant predation rate without satiety when voles peaked. The predation impact on microtines was positively dependent on vole densities and suggests that the owls dampen microtine cycles. The following factors seemed to promote the dampening impact: rapid numerical and functional responses to changes in vole densities, owl populations only slightly limited by territoriality, and spatial heterogeneity of the study area.

FOOD LIMITATION ON BROOD SIZE: EXPERIMENTAL EVIDENCE IN THE EURASIAN KESTREL

Food limitation on reproduction during the nestling stage was experimentally tested in a Finnish population of Eurasian Kestrels (Falco tinnunculus). Nests were provided with supplemental food from hatching to fledging for three years (1992, 1993, and 1995), which differed in the natural abundance of voles, the Eurasian Kestrels major prey. These supplemented nests were compared to nonsupplemented control nests using the following variables: (1) parental effort, (2) parental condition, and (3) fledgling number and quality. Female parents responded to food supplements by decreasing their hunting effort (estimated as the percentage of time spent flight-hunting) and prey delivery rate, whereas the hunting effort and/or prey delivery rate of males did not change. Females at supplemented nests were heavier than those at control nests, but the body mass of males was not affected by feeding. Supplementary food increased the number of fledglings per brood not only in years of low, but also in years of relatively high natural prey density. We conclude that even at high levels of natural food abundance, the reproductive output of kestrels is food-limited during the nestling period. In addition, there appear to be intersexual differences in the adjustment of parental effort. While females adjusted parental effort to male provisioning and offspring requirements, males did not change parental- effort within a season, suggesting that male parental effort is fixed at a level where male survival is not jeopardized.