Gradients in density variations of small rodents: the importance of latitude and snow cover

Summary Microtine rodents are known to show extreme population variations (cycles) but non-cyclic populations have also been recognized during recent years. The cyclic populations have been widely thought to be regulated by intrinsic mechanisms. However, such predictions for cyclic populations are usually not applicable to non-cyclic ones and extrinsic factors may have to be included in any explanation.A hypothesis that the degree of fluctuations in small rodent numbers is related to the sustainable number of generalist predators was tested on mainly literature data by computing indices of cyclicity for local populations. These indices were related to latitude and snow cover (two measures) as these variables will affect the amount of alternative prey available for these generalists. Within Fennoscandia such indices for Clethrionomys glareolus and Microtus agrestis were clearly positively related to latitude and snow cover. The fraction of populations with summer declines in numbers, characterizing highly cyclic populations, increased in the same way. Cyclicity indices in Great Britain were similar to those in southern Fennoscandia, both areas being poor in snow, but were higher at the same latitudes in eastern Europe with more snow. Indices of density variations were generally low in North American Clethrionomys species and very variable in Microtus species.The gradients observed and differences between continents are interpreted as due to microtine-vegetation interactions in northern European areas poor in generalist predators but with important small mustelid predation, and to similar snowshoe hare-vegetation interactions in mainly Canada-Alaska, where small rodents may serve as alternative prey for numerically fluctuating hare predators, at least in the forests. Western European microtine populations, and probably many others, seem to be regulated by generalist predators.     

Clutch size and breeding success in relation to nest-box size in Tengmalm's owl Aegolius funereus

Clutch size and breeding success was related to nest-box size in 215 nests of Tengmalm's owl in the Kauhava region, western Finland in 1966–82. In vole peak years, but not in other years, mean clutch size was positively correlated with the bottom area of the nest-box, increasing on average by 0.005 eggs cm⁻². In successful nests there were fewer nestlings in small and medium-sized than in large boxes. Breeding was most successful in thick-walled boxes with a small entrance diameter. The optimal box for Tengmalm's owl has the following dimensions: bottom area 20 × 20 cm, entrance diameter 8 cm, and wall thickness at least 3 cm.
Hypotheses suggested to explain the "area effect" based on breeding data of hole-nesting passerines do not hold good for Tengmalm's owl. Since there were more stored prey animals in medium-sized and large boxes than in small boxes, I suggest that the "area effect" is related to food availability, which may determine how sensitive the species is to different bottom areas of the boxes, at least in areas with cyclic food (e.g. northern Europe).     

Timing of breeding of Tengmalm's Owl Aegolius funereus in relation to vole dynamics in western Finland

Timing of breeding in Tengmalm's Owl was studied in western Finland for 13 years. During 1973-85, half of the females started laying before 4 April, near the seasonal low of main food abundance (voles), and earlier than in southern Finland or as early as in southeastern Norway. The reason for this latitudinal trend is the shallow snow cover of the study area. The annual variation in the median laying dates was one month and was negatively correlated with the spring abundance of Microtus voles. The mean clutch size was related to the start of laying with early clutches being larger than late ones. These findings accord with the 'food limitation hypothesis', which states that laying begins as soon as the female can accumulate enough energy stores for forming eggs. Early breeding is adaptive, since juveniles of early clutches probably survive better during their first winter. In adults, early nesting improves the chances of rearing two broods per year, allows them to moult after breeding and gives more time to accumulate fat reserves to survive the winter. Tengmalm's Owl is one of the earliest breeders among North European birds. This is possible because of its hole-nesting and resident habits, small body-size in relation to the main prey and the greatest sexual size dimorphism among European owls.     

Residency,migration and a compromise: Adaptations to nest-site scarcity and food specialization in three fennoscandian owl species

Summary Fennoscandian owl species differ, among other things, with respect to nest-site, food, clutch size, mate and territory fidelity, sexual size dimorphism and longevity. All these life characteristics help shaping the pattern of mobility and wintering strategies found in owl species, but it seems justifiable to regard food abundance and nest-site availability as the most prominent ones.The Ural owl is a generalist feeder and nests in tree cavities which are scarce. The pair is faithful to their territory for life. The long-eared owl is a vole specialist, breeds in secondhand twig-nests, which are abundantly available, and is largely migratory. Tengmalm's owl is a vole specialist and breeds in tree holes. As an adaptation to the conflicting pressures of periodical food scarcity and of keen competition for the nest holes which therefore have better be guarded uninterruptedly this species has evolved a strategy of partial migration, adult males being resident and females and young being migratory.     

Is the heart of Fennoscandian rodent cycle still beating? A 14‐year study of small mammals and Tengmalm's owls in northern Norway

Analyses of spatial and temporal patterns of the small mammal cycle in Fennoscandia have led to two main conclusions: a south-north geographical gradient in the strength of density dependence and period length, and a change in temporal dynamics with less clear periodicity and lower amplitude of fluctuations in recent years. Fourteen years (1985–1998) of small mammals trapping and Tengmalm's owls monitoring data provided clear evidence for 3-yr cycles of two vole species in inner Troms, north Norway, at the same latitude and only 80 km from Kilpisjärvi, north Finland, where 4–5-yr cycles have been the norm until the end of 1980s. The response of Tengmalm's owls to variation in small rodents abundance was not delayed, as was observed in central Finland. Common shrews appeared to have more stable dynamics. The features of the cycle, and a reassessment of the previously described patterns, show that the dynamics may be different over short distances. Furthermore, snow cover and habitat fragmentation should explicitly be taken into account in any understanding of the Fennoscandian gradient, and surrogate variables such as latitude should be avoided. We stress the need for a more extensive coverage of spatial and temporal patterns in cyclicity with respect to assumed ecological causes.     

Factors promoting polygyny in European birds of prey—a hypothesis

Summary Polygyny is known in at least nine (out of 36) European raptor (Accipitriformes and Falconiformes) and seven (out of 13) owl (Strigiformes) species that hunt mobile prey. The hypothesis put forward here suggests that abundant food supply and nomadic tactics of breeding dispersal are crucial factors promoting polygyny in birds of prey. The hypothesis predicts that: (1) polygyny is more common in rodent-eating birds of prey than in bird-eating ones; (2) polygyny is more frequent in good vole years than in poor ones; (3) the frequency of polygyny in vole-eating species should increase northwards in Europe, as the densities of voles in the peak phase increase in that direction; (4) the frequency of polygyny and harem size should be increased by supplementary feeding; and (5) polygyny is more common in nomadic birds of prey with annual pair bonds and weak territoriality than in resident birds of prey with longerterm pair bonds and stronger territoriality. A majority of the available data is consistent with predictions 1–3 and 5, but data on prediction 4 are scanty. Further studies on ringed birds of prey are needed to test the validity of the hypothesis.     

Vole population cycles in northern and southern Europe: is there a need for different explanations for single pattern?

1. Students of population cycles in small rodents in Fennoscandia have accumulated support for the predation hypothesis, which states that the gradient in cycle length and amplitude running from southern to northern Fennoscandia reflects the relative influence of specialist and generalist predators on vole dynamics, itself modulated by the presence of snow cover. The hypothesized role of snow cover is to isolate linked specialist predators, primarily the least weasel, Mustela n. nivalis L. and their prey, primarily field voles Microtus agrestis L., from the stabilizing influence of generalist predators. 2. The predation hypothesis does not readily account for the high amplitude and regular 3-year cycles of common voles documented in agricultural areas of western, central and eastern Europe. Such cycles are rarely mentioned in the literature pertaining to Fennoscandian cycles. 3. We consider new data on population cycles and demographic patterns of common voles Microtus arvalis Pallas in south-west France. We show that the patterns are wholly consistent with five of six patterns that characterize rodent cycles in Fennoscandia and that are satisfactorily explained by the predation hypothesis. They include the: (a) existence of cycle; (b) the occurrence of long-term changes in relative abundance and type of dynamics; (c) geographical synchrony over large areas; (d) interspecific synchrony; and (e) voles are large in the increase and peak phase and small in decline and low phase, namely. There is a striking similarity between the patterns shown by common vole populations in south-west France and those from Fennoscandian cyclic rodent populations, although the former are not consistent with a geographical extension of the latitudinal gradient south of Fennoscandia. 4. It is possible that the dominant interaction leading to multiannual rodent oscillations is different in different regions. We argue, however, that advocates of the predation hypothesis should embrace the challenge of developing a widely applicable explanation to population cycles, including justifying any limits to its applicability on ecological and not geographical grounds.     

Fasting endurance and cold resistance without hypothermia in a small predatory bird: the metabolic strategy of Tengmalm's owl,Aegolius funereus

The energetic adaptations of non-breeding Tengmalm's owls (Aegolius funereus) to temperature and fasting were studied during the birds' autumnal irruptions in western Finland. Allometric analysis (including literature data and two larger owl species measured in this study) indicates that the basal metabolic rate of owls is below the mean level of non-passerine birds. However, the basal metabolic rate of the 130-g Tengmalm's owl (1.13 W) is higher than in other owls of similar size. This is probably related to its northern distribution and nomadic life history. Relative to its size, Tengmalm's owl has excellent cold resistance due to effective insulation (lower critical temperature +10°C, minimum conductance 0.19 mW·cm^-2·°C^-1). Radiotelemetric measurements of body temperature showed that the level of body temperature is lower than for birds in general (39.4°C at zero activity) and that the amplitude of the diurnal cycle is also low (0.2–0.6°C). In contrast to many other small birds, Tengmalm's owls do not enter hypothermia during a 5-day fast at thermoneutrality or in cold. Moreover, while the metabolic rate per bird shows the expected mass-dependent decrease, the mass-specific rate decreases only slightly during the fast. In line with this, there was no decrease in the plasma triiodothyronine concentration during the fast in the owl, whereas a dramtic drop was observed in the pigeon and Japanese quail that were used as a reference. Despite this, the owl has an excellent capacity for fasting because of its ability to accumulate extensive fat depots and its low overall metabolic rate. Fasting reduced evaporative water loss to 50% of that in the fed state. Calculations show that the oxygen consumption observed in fasting birds would involve a production of metabolic water barely sufficient to compensate for evaporative water loss. The threat of dehydration may thus set a limit to the decrease in metabolic rate in fasting owls (owls rely totally on water either ingested with food or produced metabolically). We conclude that the metabolic strategy in Tengmalm's owl is largely dictated by an evolutionary pressure for fasting endurance. With the restrictions set by small body size and water economy, this bird has apparently taken these adaptations to an extreme. The constraints that preclude hypothermia, which could increase the capacity for fasting even more, remain unknown.Abbreviations BM body mass - BMR basal metabolic rate - EWL vaporative water loss - MR metabolic rate - T₃ triiodothyronine - T _a ambient temperature - T _b body temperature - VO₂ oxygen consumption     

Refuge sites of voles under owl predation risk: priority of dominant individuals?

In an aviary experiment, we studied whether body size or habitatfamiliarity of field voles (Microtus agrestis) affected predationrisk by Tengmalm's owls (Aegolius funereus). In the field, wecompared the body size of field voles snap-trapped in good (covered)and poor (open) habitats in 1992 and 1994 to determine whetherthere were habitat-related differences in the body size of voles.In the aviary, large individuals occupied the good habitat significantlymore than small individuals both in the control (owl not present)and experimental treatments (owl present). Furthermore, habitat-familiarvoles inhabited the good habitat more than habitat-unfamiliarvoles did when an owl was present Our field data were consistentwith our aviary data: larger field voles were more frequentlyfound in good habitats than in poor habitats. In the aviary,Tengmalm's owl predation risk was higher for small and habitat-unfamiliarvoles. This suggests that large field voles may have priorityto sheltered habitats. Furthermore, habitat familiarity mayplay a central role in avoiding risky habitats.     

Fading out of vole and predator cycles?

Northern voles and lemmings are famous for their spectacular multiannual population cycles with high amplitudes. Such cyclic vole populations in Scandinavia have shown an unexpected and marked long-term decline in density since the early 1970s, particularly with a marked shift to lower spring densities in the early 1980s. The vole decline, mainly characterized by a strongly decreased rate of change in numbers over winter, is associated with an increased occurrence of mild and wet winters brought about by a recent change in the North Atlantic Oscillation. This has led to a decrease in winter stability and has shortened the period with protective snow cover, the latter considered as an important prerequisite for the occurrence of multiannual, high-amplitude cycles in vole populations. Although the vole decline is predicted to be negative for predators' reproduction and abundance, empirical data showing this are rare. Here we show that the dynamics of a predator-prey system (Tengmalm's owl, Aegolius funereus, and voles), have in recent years gradually changed from 3-4 yr, high-amplitude cycles towards more or less annual fluctuations only.     

Interspecific competition limits larders of pygmy owls Glaucidium passerinum

To test whether competitive and predatory interactions limit larder size we erected pygmy owl Glaucidium passerinum nest-boxes for hoarding with 45 mm entrance diameter near and far (>2 km) from Tengmalm's owl Aegolius funereus nest-boxes with >80 mm entrance diameter during early autumn. We found larders of pygmy owls in similar frequency in both near and far plots (41 vs. 42% of plots), but in near plots the number and biomass of cached prey by pygmy owls were lower. These results suggest that there is competition for food between these two owl species and/or that food caching behaviour of pygmy owls is disturbed by larger Tengmalm's owls.     

Effect of snow cover on seasonal changes in diet, habitat, and regional distribution of raptors that prey on small mammals in boreal zones of Fennoscandia

Seasonal changes in spatial distribution of search effort of birds that prey on small mammals were studied in two structurally different coniferous forest habitats in the northern boreal zone in SE Norway. During the season with snow cover both the proportion of Microtus relative to that of Clethrionomys in the predators' diet, and their use of a clear-cut relative to that of older forest were lower than during the snow-free season. This was related to a lower relative availability of prey ( Microtus agrestis and M. oeconomus ) in the clear-cut when the ground was snow-covered than when it was snow-free. Based on this local pattern I suggest the following explanation for differences in migratory strategy between raptors that prey on small mammals in Fennoscandian boreal zones: species that migrate to snow-free areas in winter are either adapted to hunt by the energetically expensive method of quartering in open grassland habitats, where prey ( Microtus ) availability is relatively low during periods with snow cover (hen harrier Circus cyaneus , short-eared owl Asio flammeus , and longeared owl A. otus ), or by sit-and-wait in open grassland and forest habitats, the latter with relatively high prey availability during periods with snow cover, but unable to locate concealed prey (kestrel Falco tinnuculus , common buzzard Buteo huteo , and roughlegged buzzard B. lagopus ). In contrast, species that remain in areas with permanent snow cover during winter use the energetically cheap sit-and-wait tactic, and are able to hunt in closed forest habitat and localize concealed prey (the remaining owl species). Interspecific differences in prey availability as determined by hunting habitat and hunting mode is probably more important in shaping the migration patterns of Fennoscandian owls than is nest site availability.     

Wintering space use and site fidelity in a nomadic species,the snowy owl

Migratory species can exploit many habitats over vast geographic areas and adopt various patterns of space and habitat use throughout their annual cycle. In nomadic species, determinants of habitat use during the non‐breeding season are poorly known due to the unpredictability of their movement patterns. Here, we analysed variability in wintering space and habitat use by a highly nomadic species, the snowy owl, in eastern North America. Using 21 females tracked by satellite telemetry between 2007 and 2016, we 1) assessed how space use patterns in winter varied according to the type of environment (marine vs terrestrial), latitudinal zone (Arctic vs temperate), local snow conditions and lemming densities and 2) investigated winter habitat and site fidelity. Our results confirmed a high inter‐individual variation in patterns of habitat use by wintering snowy owls. Highly‐used areas were concentrated in the Arctic and in the marine and coastal environments. Owls wintering in the marine environment travelled over longer distances during the winter, had larger home ranges and these were divided in more smaller zones than individuals in terrestrial environments. Wintering home range sizes decreased with high winter lemming densities, use of the marine environment increased following high summer lemming densities, and a thick snow cover in autumn led to later settlement on the wintering ground. Contrary to expectations, snowy owls tended to make greater use of the marine environment when snow cover was thin. Snowy owls were highly consistent in their use of a given wintering environment and a specific latitudinal zone between years, but demonstrated flexibility in their space use and a modest site fidelity. The snowy owls’ consistency in wintering habitat use may provide them with advantages in terms of experience but their mobility and flexibility may help them to cope with changing environmental conditions at fine spatial scale.     

Owl winter irruptions as an indicator of small mammal population cycles in the boreal forest of eastern North America

Contrary to what is observed in Fennoscandia, it seems to be widely accepted that small mammals do not exhibit multi-annual population cycles in the boreal forest of North America. However, in the last thirty years, irruptions of vole predators such as owls have been reported by ornithologists south of the North American boreal forest. While such southerly irruptions have been associated in Fennoscandia with periods of low abundance of small mammals within their usual distribution range, their possible cyclic nature and their relationships to fluctuations in vole densities at northern latitudes has not yet been demonstrated in North America. With information collected from existing data-bases, we examined the presence of cycles in small mammals and their main avian predators by using temporal autocorrelation analyses. Winter invasions of boreal owls ( Aegolius funereus ) were periodic, with a 4-yr cycle in Québec. Populations of one species of small mammal, the red-backed vole ( Clethrionomys gapperi ), fluctuated periodically in boreal forests of Québec (north to 48°N). Boreal owls show invasion cycles which correspond to years of low density of red-backed voles, the main food item for this owl species. In addition, winter observations of northern hawk owls ( Surnia ulula ) and great gray owls ( Strix nebulosa ) south of their usual range increased in years of low density of red-backed voles. Our results suggest that a 4-yr population cycle exists in the eastern boreal forest of North America for voles and owls, which is very similar to the one observed in Fennoscandia.     

Climate change and perishable food hoards of an avian predator: Is the freezer still working?

Changing climate can modify predator–prey interactions and induce declines or local extinctions of species due to reductions in food availability. Species hoarding perishable food for overwinter survival, like predators, are predicted to be particularly susceptible to increasing temperatures. We analysed the influence of autumn and winter weather, and abundance of main prey (voles), on the food‐hoarding behaviour of a generalist predator, the Eurasian pygmy owl (Glaucidium passerinum), across 16 years in Finland. Fewer freeze–thaw events in early autumn delayed the initiation of food hoarding. Pygmy owls consumed more hoarded food with more frequent freeze–thaw events and deeper snow cover in autumn and in winter, and lower precipitation in winter. In autumn, the rotting of food hoards increased with precipitation. Hoards already present in early autumn were much more likely to rot than the ones initiated in late autumn. Rotten food hoards were used more in years of low food abundance than in years of high food abundance. Having rotten food hoards in autumn resulted in a lower future recapture probability of female owls. These results indicate that pygmy owls might be partly able to adapt to climate change by delaying food hoarding, but changes in the snow cover, precipitation and frequency of freeze–thaw events might impair their foraging and ultimately decrease local overwinter survival. Long‐term trends and future predictions, therefore, suggest that impacts of climate change on wintering food‐hoarding species could be substantial, because their ‘freezers’ may no longer work properly. Altered usability and poorer quality of hoarded food may further modify the foraging needs of food‐hoarding predators and thus their overall predation pressure on prey species. This raises concerns about the impacts of climate change on boreal food webs, in which ecological interactions have evolved under cold winter conditions.     

Large-scale geographic patterns of genetic variation in Melica nutans, a widespread Eurasian woodland grass

 The geographic distribution of allozyme variation within the Eurasian boreo-nemoreal woodland grass Melica nutans L. has been investigated together with a minor subset of other Melica species. Twenty alleles were found at nine polymorphic loci in M. nutans. Allelic richness was highest in areas central in the species' European distribution, i.e. in southern Fennoscandia. High population densities, reducing the effects of genetic drift, as well as accumulation of variation through long-distance gene-flow from different marginal populations, is proposed to explain high allelic richness in this area. Several alleles showed geographic patterns in distribution and frequency variation. However, these patterns were not congruent, e.g. some alleles appear to have migrated to northern Europe from the south-west whereas others may have spread from the east. Genetic distances between geographic regions, each consisting of 2–6 populations, were generally low between all Fennoscandian, Russian and Siberian regions, but much higher between western and continental European regions. On the population level, cluster analysis grouped populations from Siberia, Russia, coastal and lowland areas in Fennoscandia and British Cumbria into one subcluster whereas other subclusters contained mainly south-west European populations or populations from almost throughout the distribution range. A scenario with several independent glacial refugia in central Europe, south-western Siberia and possibly western Norway, and subsequent colonisation of Fennoscandia mainly from the east, but with some long-distance gene-flow from central Europe, is proposed. Received April 3, 2002; accepted September 17, 2002 Published online: December 11, 2002     

Food web structure and climate effects on the dynamics of small mammals and owls in semi-arid Chile

Population dynamics of small mammals and predators in semi-arid Chile is positively correlated with rainfall associated with incursions of El Niño (El Niño Southern Oscillation: ENSO). However, the causal relationships between small mammal fluctuations, predator oscillations, and climatic disturbances are poorly understood. Here, we report time series models for three species of small mammal prey and two species of owl predators. The large differences in population fluctuations between the three small mammal species are related to differences in their respective feedback structures. The analyses reveal that per capita growth rate of the leaf-eared mouse is a decreasing function of log density and of log barn owl abundance together with a positive rainfall effect. In turn, per capita population growth rate ( R -function) of the barn owl is a negative function of log barn owl abundance and a positive function of leaf-eared mouse abundance, suggesting a predator–prey interaction. The dramatic population fluctuations exhibited by leaf-eared mouse ( Phyllotis darwini ) are caused by climate effects coupled with a complex food web architecture.     

Specialist and generalist natural enemies as an explanation for geographical gradients in population cycles of northern herbivores

Within Fennoscandia, two well-studied groups of herbivores exhibit clear geographical gradients in their population dynamics. Populations of a forest lepidopteran ( Epirrita autumnata , the autumnal moth) and voles of the genera Microtus and Clethrionomys show pronounced multi-annual cycles in the north but become more stable towards the south. Here we review empirical and theoretical studies on these species, mainly regarding the biological mechanisms that are assumed to generate the pattern of population dynamics in both systems. We conclude that the specialist/generalist predation hypothesis offers a common explanation for the population cycles and their geographical gradients irrespective of whether a herbivorous insect or small mammals are concerned. According to this hypothesis, originally developed for the Fennoscandian voles, but now applied also to E. autumnata , population cycles are generated by specialist natural enemies (predators for the voles and parasitoids for E. autumnata ). Furthermore, the dynamic shift from cycles to stability is assumed to be caused by an increase in the density and diversity of generalist natural enemies from north to south in Fennoscandia.     

Demographic responses to a mild winter in enclosed vole populations

Mild winter weather causing snow to melt and ice to accumulate on the ground has been proposed to cause the decreased survival of individuals, and less pronounced cyclicity, of small rodent populations in Fennoscandia. However, detailed data linking ice accumulation to decreased winter survival is lacking. We live-trapped and monitored with passive integrated transponders enclosed populations of root voles (Microtus oeconomus) exposed to different amounts of ice accumulation through a mild winter. We studied how social behaviour and survival responded to snow melt and ice accumulation. Voles avoided ground ice by moving their home ranges, thus increasing home range overlap in enclosed populations experiencing more extensive ice cover. Winter survival was not affected by the amount of ice accumulation, and was only slightly reduced during ice formation in early winter. The lowest survival rates were found at the onset of snow melt in early spring. These results suggest that ice accumulation does not cause lower survival during mild winters, probably because plastic social behaviour enables root voles to reduce the negative effects of varying winter weather on survival. The mechanisms for lower survival during mild winters may operate during spring and be related to spring floods or increased susceptibility to predators. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Hatching asynchrony and brood reduction in Tengmalm's owl <Emphasis Type="Italic">Aegolius funereus</Emphasis>: the role of temporal and spatial variation in food abundance

Hatching asynchrony is the consequence of birds initiating incubation before clutch completion. It has been suggested that variation in hatching asynchrony in owls is extensive, and therefore they should be excellent objects to study the effects of spatio-temporal variation in food abundance on this phenomenon. We examined how abundance and predictability of food affected hatching asynchrony in Tengmalm's owl Aegolius funereus (Linnaeus), which mainly feeds on voles which fluctuate in 3- to 4-year cycles in northern Europe. Hatching span averaged 6-7 days (range 0-13 days) and increased with clutch size. Food supply did not directly influence levels of hatching asynchrony but it influenced indirectly via marked among-year changes in clutch size. During the decrease phase of the vole cycle the proportion of hatchlings producing fledglings decreased with asynchrony, suggesting that chick mortality was most common among asynchronous broods when food became scarce. This finding is consistent with Lack's brood reduction hypothesis, i.e. that if food becomes scarce during the nestling period the youngest nestlings would die first without endangering the survival of the whole brood.