Kai Norrdahl

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.

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.

Population cycles in northern small mammals.

I. The regular multiannual oscillations of small mammals at northern latitudes have been a subject of intensive study from the beginning of this century. The existence of a subjective bias in the research due to different schools of study together with a long series of failures and seemingly contradictory results in experiments testing a multitude of hypotheses have brought confusion to the field of study. Much of this confusion has resulted from a failure to recognize sharply the problem studied, which in turn has masked the progress made during the years. Northern mammal cycles are not a single problem but a composition of many related problems. Every problem may have a single-factor explanation, but even with a single-factor explanation, one factor is not necessarily an answer to all of the related problems. 2. At present, we can state that the cyclicity is caused by a predator-prey interaction. Both the 8-11-year and the 3-5-year cycles may be special cases of a more general cycle, most likely caused by a herbivore-resident specialist predator interaction, where the period of the cycles is determined by size-related constraints affecting the increase rate of the populations. The factors determining the amplitude of the cycles probably vary regionally and/or temporally. The operation of generalist and nomadic predators is largely responsible for the regional and geographic synchrony in cycles, although climatic factors may also contribute to the geographic synchrony. The northern distribution of animal communities; both these factors affect the density of generalist predators, which act as a stabilizing factor in the system. The age-related survival pattern seems to be mainly caused by predation, and the cyclically fluctuating reproductive output and mean body mass may be caused by changes in prey behaviour in response to fluctuating predation risk. Thus, we can already give a plausible explanation for most problems related to northern mammal cycles. 3. In all problems discussed, predation seems to be involved, and in most problems, it seems to be the factor which explains the observed patterns. Thus, as a generalization, it can be said that predation seems to be the key factor in the explanation of the northern multiannual cycles of small mammals. 4. There seems to be a linkage between diversity and cyclicity, probably because the diversity of the community (the number of prey species available) may determine the diet choice of a predator, which in turn determines whether the predators have a stabilizing or a destabilizing impact on prey populations.(ABSTRACT TRUNCATED AT 400 WORDS)

Predator–induced synchrony in population oscillations of coexisting small mammal species

Comprehensive analyses of long–term (1977–2003) small–mammal abundance data from western Finland showed that populations of Microtus voles (field voles M. agrestis and sibling voles M. rossiaemeridionalis), bank voles (Clethrionomys glareolus) and common shrews (Sorex araneus) fluctuated synchronously in 3 year population cycles. Time–series analyses indicated that interspecific synchrony is influenced strongly by density–dependent processes. Synchrony among Microtus and bank voles appeared additionally to be influenced by density–independent processes. To test whether interspecific synchronization through density–dependent processes is caused by predation, we experimentally reduced the densities of the main predators of small mammals in four large agricultural areas, and compared small mammal abundances in these to those in four control areas (2.5–3 km2) through a 3 year small–mammal population cycle. Predator reduction increased densities of the main prey species, Microtus voles, in all phases of the population cycle, while bank voles, the most important alternative prey of predators, responded positively only in the low and the increase phase. Manipulation also increased the autumn densities of water voles (Arvicola terrestris) in the increase phase of the cycle. No treatment effects were detected for common shrews or mice. Our results are in accordance with the alternative prey hypothesis, by which predators successively reduce the densities of both main and alternative prey species after the peak phase of small–mammal population cycles, thus inducing a synchronous low phase.

Experimental tests of predation and food hypotheses for population cycles of voles

Pronounced population cycles are characteristic of many herbivorous small mammals in northern latitudes. Although delayed density–dependent effects of predation and food shortage are often proposed as factors driving population cycles, firm evidence for causality is rare because sufficiently replicated, large–scale field experiments are lacking. We conducted two experiments on Microtus voles in four large predator–proof enclosures and four unfenced control areas in western Finland. Predator exclusion induced rapid population growth and increased the peak abundance of voles over 20–fold until the enclosed populations crashed during the second winter due to food shortage. Thereafter, voles introduced to enclosures which had suffered heavy grazing increased to higher densities than voles in previously ungrazed control areas which were exposed to predators. We concluded that predation inhibits an increase in vole populations until predation pressure declines, thus maintaining the low phase of the cycle, but also that population cycles in voles are not primarily driven by plant–herbivore interactions.

WINTER FOOD SUPPLY LIMITS GROWTH OF NORTHERN VOLE POPULATIONS IN THE ABSENCE OF PREDATION

Mathematical models have suggested that population cycles of northern voles are generated by a combined effect of delayed and direct density-dependent mechanisms. Predation is considered to be the most likely mechanism affecting vole populations in a delayed density-dependent manner. We conducted a replicated two-factor experiment with the field vole (Microtus agrestis) during 1999-2001 in western Finland, manipulating both predation rate and winter food supply to evaluate whether a shortage of winter food has the potential to limit the growth of vole populations in a direct density-dependent manner. Vole populations in fenced predator exclosures rapidly attained higher densities than in unfenced areas, with the difference persisting until the end of the experiment. In the first winter, food supplementation increased vole population growth in fenced areas, but not in unfenced areas. The growth of vole populations in both supplemented and nonsupplemented fenced areas became limited in a direct density-dependent manner during the first winter. During the second winter, food supplementation prevented the crash of vole populations within fences, whereas again no obvious effect was found in the areas exposed to predation. Furthermore, supplemental winter food increased the overwinter survival of voles in fenced areas in both winters. Our results indicate that Microtus vole populations that have succeeded in escaping regulation by predators are limited in growth by a lack of winter food. This factor is thus a strong candidate for the direct density dependence inherently necessary for the occurrence of population cycles.

Do breeding nomadic avian predators dampen population fluctuations of small mammals

The mean consumption of all prey by adult and young European kestrels (EKs), shot-eared owls (SOs) and long-eared owls (LOs) in one breeding season was (±S.D.) 585±525 kg in 47 km 2 of farmland area in western Finland during 1977-87. The proportion of prey consumption was highest by EKs (50), followed by SOs (36%) and LOs (14%). The voles (Microtu agrestis and M. epiroticus) were the most frequent prey taken by the three species of birds of prey, though in vole lows shrews and small birds were the most abundant prey. In good vole years, Microtus voles suffered from a heavier predation than bank voles and common shrews, but the contrary was true in poor vole years when numbers of birds of prey were low