Subnivean Space Research Articles

Radon as a possible link between peak spring tides and lemming cycles

There is still no consensus regarding the ultimate cause of the famous 3–4-year population cycles of lemmings. According to the plant stress hypothesis, herbivore population peaks are caused by stress factors that force plants to reallocate stored defensive proteins to transportable and easily digestible N-compounds. One possible plant stress factor is ionization caused by exhalation of the radioactive noble gas radon, which is enhanced after spring tides, i.e., tides at new or full Moon. I hypothesized that increased ionization caused by radon accumulation in the subnivean space after peak spring tides, which occur close to perihelion (31 December–05 January, when the Earth–Sun distance is shortest), and at 3.8-year intervals, results in increased protein digestibility of mosses, which are important food for lemmings. Population outbreaks of Norway lemming Lemmus lemmus occurred two years after peak spring tides during 1871–1910, when also perigee (the time when the Earth–Moon distance is shortest) coincided with spring tides and perihelion. Thereafter this relationship weakened, and lemming peaks became less pronounced and more related to plant seed indices. As we have now entered a new 30-year period with coincidence of spring tide, perihelion and perigee, I predict more regular and pronounced lemming outbreaks in the next decades, unless radon accumulation is prevented by frequent lack of a stable snow cover due to global warming.

Spatiotemporally variable snow properties drive habitat use of an Arctic mesopredator.

Climate change is rapidly altering the composition and availability of snow, with implications for snow-affected ecological processes, including reproduction, predation, habitat selection, and migration. How snowpack changes influence these ecological processes is mediated by physical snowpack properties, such as depth, density, hardness, and strength, each of which is in turn affected by climate change. Despite this, it remains difficult to obtain meaningful snow information relevant to the ecological processes of interest, precluding a mechanistic understanding of these effects. This problem is acute for species that rely on particular attributes of the subnivean space, for example depth, thermal resistance, and structural stability, for key life-history processes like reproduction, thermoregulation, and predation avoidance. We used a spatially explicit snow evolution model to investigate how habitat selection of a species that uses the subnivean space, the wolverine, is related to snow depth, snow density, and snow melt on Arctic tundra. We modeled these snow properties at a 10m spatial and a daily temporal resolution for 3 years, and used integrated step selection analyses of GPS collar data from 21 wolverines to determine how these snow properties influenced habitat selection and movement. We found that wolverines selected deeper, denser snow, but only when it was not undergoing melt, bolstering the evidence that these snow properties are important to species that use the Arctic snowpack for subnivean resting sites and dens. We discuss the implications of these findings in the context of climate change impacts on subnivean species.

Direct and indirect effects of regional and local climatic factors on trophic interactions in the Arctic tundra

Climate change can impact ecosystems by reshaping the dynamics of resource exploitation for predators and their prey. Alterations of these pathways could be especially intense in ecosystems characterized by a simple trophic structure and rapid warming trends, such as in the Arctic. However, quantifying the multiple direct and indirect pathways through which climate change is likely to alter trophic interactions and their relative strength remains a challenge. Here, we aim to identify direct and indirect causal mechanisms driven by climate affecting predator-prey interactions of species sharing a tundra food web. We based our study on relationships between one Arctic predator (Arctic fox) and its two main prey - lemmings (preferred prey) and snow geese (alternate prey) - which are exposed to variable local and regional climatic factors across years. We used a combination of models mapping multiple causal links among key variables derived from a long-term dataset (21years). We obtained several possible scenarios linking regional climate factors (Arctic oscillations) and local temperature and precipitation to the breeding of species. Our results suggest that both regional and local climate factors have direct and indirect impacts on the breeding of foxes and geese. Local climate showed a positive causal link with goose nesting success, while both regional and local climate displayed contrasted effects on the proportion of fox breeding. We found no impact of climate on lemming abundance. We observed positive relationships between lemming, fox and goose reproduction highlighting numerical and functional responses of fox to the variability of lemming abundance. Our study measures causal links and strength of interactions in a food web, quantifying both numerical response of a predator and apparent interactions between its two main prey. These results improve our understanding of the complex effects of climate on predator-prey interactions and our capacity to anticipate food web response to ongoing climate change.

The Effects of Winter Climate and Intrinsic Factors on Survival of Cyclic Vole Populations in Southeastern Norway

Changes in winter climate is a possible explanation for dampened population cycles in voles. For voles living in the subnivean space for several months of the year, we may expect that winter conditions affect survival. We examined the effect of different winter climate descriptors (snow depth, subnivean temperature, snow crust) and different intrinsic factors (sex, age, physiology, behaviour estimated as the longest distance travelled between traps) on winter survival of bank voles Myodes glareolus in southeastern Norway by live-trapping voles monthly along elevation gradients. We tested whether winter conditions alone (winter hypothesis), intrinsic factors alone (intrinsic hypothesis), or winter conditions in combination with age and sex were more important for winter survival of voles (multiple factor hypothesis). Our results do not support the winter hypothesis as there were no relations between winter survival and snow depth, snow crust and subnivean temperature. We found strongest support for the intrinsic hypothesis, where the distance travelled was positively correlated with survival. We hypothesize that this behavioural descriptor is related to food resources and their importance during winter, where an increased activity range (distance travelled between traps) increase the access to food resources.

Surviving winter: Food, but not habitat structure, prevents crashes in cyclic vole populations.

Vole population cycles are a major force driving boreal ecosystem dynamics in northwestern Eurasia. However, our understanding of the impact of winter on these cycles is increasingly uncertain, especially because climate change is affecting snow predictability, quality, and abundance. We examined the role of winter weather and snow conditions, the lack of suitable habitat structure during freeze‐thaw periods, and the lack of sufficient food as potential causes for winter population crashes. We live‐trapped bank voles Myodes glareolus on 26 plots (0.36 ha each) at two different elevations (representing different winter conditions) in southeast Norway in the winters 2013/2014 and 2014/2015. We carried out two manipulations: supplementing six plots with food to eliminate food limitation and six plots with straw to improve habitat structure and limit the effect of icing in the subnivean space. In the first winter, all bank voles survived well on all plots, whereas in the second winter voles on almost all plots went extinct except for those receiving supplemental food. Survival was highest on the feeding treatment in both winters, whereas improving habitat structure had no effect. We conclude that food limitation was a key factor in causing winter population crashes.

The importance of bank vole density and rainy winters in predicting nephropathia epidemica incidence in Northern Sweden.

Pathogenic hantaviruses (family Bunyaviridae, genus Hantavirus) are rodent-borne viruses causing hemorrhagic fever with renal syndrome (HFRS) in Eurasia. In Europe, there are more than 10,000 yearly cases of nephropathia epidemica (NE), a mild form of HFRS caused by Puumala virus (PUUV). The common and widely distributed bank vole (Myodes glareolus) is the host of PUUV. In this study, we aim to explain and predict NE incidence in boreal Sweden using bank vole densities. We tested whether the number of rainy days in winter contributed to variation in NE incidence. We forecast NE incidence in July 2013–June 2014 using projected autumn vole density, and then considering two climatic scenarios: 1) rain-free winter and 2) winter with many rainy days. Autumn vole density was a strong explanatory variable of NE incidence in boreal Sweden in 1990–2012 (R2 = 79%, p<0.001). Adding the number of rainy winter days improved the model (R2 = 84%, p<0.05). We report for the first time that risk of NE is higher in winters with many rainy days. Rain on snow and ground icing may block vole access to subnivean space. Seeking refuge from adverse conditions and shelter from predators, voles may infest buildings, increasing infection risk. In a rainy winter scenario, we predicted 812 NE cases in boreal Sweden, triple the number of cases predicted in a rain-free winter in 2013/2014. Our model enables identification of high risk years when preparedness in the public health sector is crucial, as a rainy winter would accentuate risk.

Diet of the Broad-toothed RatMastacomys fuscus(Rodentia:Muridae) in the alpine zone of the Snowy Mountains, Australia

In seasonally snow-covered environments, larger mammalian species occurring above the snow have been shown to broaden diet breadth in winter, but below the snow in the subnivean space the relationship between snow cover and diet is quite different. The Broad-toothed Rat Mastacomys fuscus, an Australian cold climate endemic, is a specialist herbivore. The diet of M. fuscus in the alpine zone of the Snowy Mountains was studied over the snow-free period and in winter. M. fuscus showed a preference for monocots over dicots throughout the year, however, there was a greater diversity and evenness of plant taxa in the diet in snow-free seasons. In winter, fewer species dominated the diet, reducing the evenness as well as the diversity. Because of lack of cover from predators in the snow-free period, M. fuscus is constrained to foraging in areas with shrub cover, where access to preferred grasses may be reduced. By contrast, in the subnivean space, because of the shelter provided by the cover of snow, M. fuscus c...

Habitat selection, reproduction and predation of wintering lemmings in the Arctic

Snow cover has dramatic effects on the structure and functioning of Arctic ecosystems in winter. In the tundra, the subnivean space is the primary habitat of wintering small mammals and may be critical for their survival and reproduction. We have investigated the effects of snow cover and habitat features on the distributions of collared lemming (Dicrostonyx groenlandicus) and brown lemming (Lemmus trimucronatus) winter nests, as well as on their probabilities of reproduction and predation by stoats (Mustela erminea) and arctic foxes (Vulpes lagopus). We sampled 193 lemming winter nests and measured habitat features at all of these nests and at random sites at two spatial scales. We also monitored overwinter ground temperature at a subsample of nest and random sites. Our results demonstrate that nests were primarily located in areas with high micro-topography heterogeneity, steep slopes, deep snow cover providing thermal protection (reduced daily temperature fluctuations) and a high abundance of mosses. The probability of reproduction increased in collared lemming nests at low elevation and in brown lemming nests with high availability of some graminoid species. The probability of predation by stoats was density dependent and was higher in nests used by collared lemmings. Snow cover did not affect the probability of predation of lemming nests by stoats, but deep snow cover limited predation attempts by arctic foxes. We conclude that snow cover plays a key role in the spatial structure of wintering lemming populations and potentially in their population dynamics in the Arctic.

Linking climate change to lemming cycles

The population cycles of rodents at northern latitudes have puzzled people for centuries, and their impact is manifest throughout the alpine ecosystem. Climate change is known to be able to drive animal population dynamics between stable and cyclic phases, and has been suggested to cause the recent changes in cyclic dynamics of rodents and their predators. But although predator-rodent interactions are commonly argued to be the cause of the Fennoscandian rodent cycles, the role of the environment in the modulation of such dynamics is often poorly understood in natural systems. Hence, quantitative links between climate-driven processes and rodent dynamics have so far been lacking. Here we show that winter weather and snow conditions, together with density dependence in the net population growth rate, account for the observed population dynamics of the rodent community dominated by lemmings (Lemmus lemmus) in an alpine Norwegian core habitat between 1970 and 1997, and predict the observed absence of rodent peak years after 1994. These local rodent dynamics are coherent with alpine bird dynamics both locally and over all of southern Norway, consistent with the influence of large-scale fluctuations in winter conditions. The relationship between commonly available meteorological data and snow conditions indicates that changes in temperature and humidity, and thus conditions in the subnivean space, seem to markedly affect the dynamics of alpine rodents and their linked groups. The pattern of less regular rodent peaks, and corresponding changes in the overall dynamics of the alpine ecosystem, thus seems likely to prevail over a growing area under projected climate change.

Activity of root voles (Microtus oeconomus) under snow: social encounters synchronize individual activity rhythms

Microtine rodents usually display short-term activity rhythms synchronized by light. Social interactions have also been suggested to act as a zeitgeber, entraining individual activity, but evidence supporting this is scarce. In areas with a permanent snow cover during winter, small rodents spend most of the time in the subnivean space, between the snow cover and the ground, where they most likely are unaffected by otherwise dominating photoperiodic cues. The subnivean space, however, is fragmented, and this limits movement and may isolate individuals living just a few meters apart. These conditions provide excellent opportunities to test for the existence of social synchronization. During two winters, I experimentally decreased the subnivean fragmentation by placing out a network of corrugated aluminium sheets on the ground before snowfall, thus increasing the potential for movement and social interaction within the subnivean space. Other areas were left as controls. Intensive PIT-tag monitoring in the subnivean system provided individual activity data of root voles (Microtus oeconomus) without disturbing normal activity. The data revealed that microtines under snow displayed a free-running activity rhythm and that the activity was evenly distributed throughout the 24-h day, indicating a lack of photo-entrainment. Despite this lack of light, interacting individuals were synchronous, and pairwise synchrony decreased with decreasing potential for social interactions. These results suggest that social interactions indeed entrain microtine activity. Several possible adaptive advantages of the synchrony of microtine rodent activity have been proposed, and these theories are discussed in light of the result presented.

Immediate and short‐term responses of bird and mammal assemblages to a subalpine wildfire in the Snowy Mountains, Australia

Abstract Over 35 days in January–February 2003, wildfires burnt across much of the subalpine/alpine landscape of south‐eastern Australia, including about 70% of the land above 1500 m in the Snowy Mountains. At the time of the fire, studies of two subalpine faunal assemblages were being undertaken. The opportunity to resurvey the assemblages was taken in order to examine the immediate impact of fire in an environment where it is uncommon but predicted to occur increasingly with global warming. A study area in the Whites River Valley, where the number of bird species was counted monthly from 1996 to 2003, and weekly in late winter–spring from 2000 to 2003, was burnt in one fire. As well as the expected decrease in the number of individual birds, the fire resulted in an immediate decrease in the number of bird species, unlike in previously studied montane forest, with only the regularly wintering species plus the olive whistler and the ground‐feeding flame robin remaining. During the post‐winter avian immigration, few regular spring migrants appeared on burnt sites despite their nearby presence on the unburnt side of the valley. Five of six small mammal trapping grids were burnt. As with fires at lower altitudes, there was an immediate reduction in mammal numbers on burnt grids following the fire, but in addition, one species, Mastacomys fuscus, declined further in the ensuing 2 months both on burnt and unburnt sites. Numbers of Antechinus swainsonii and Rattus fuscipes stabilized until autumn/winter when there was a further decline due to the unavailability of subnivean space to allow winter foraging, allied with a concentration of fox predation on areas still carrying populations of small mammals.

The Characteristics and Classification of Australian Snow Cover: an Ecological Perspective

We provide a description of the structural and thermal characteristics of snow cover in the Snowy Mountains of southeast Australia. Using the snow classification system developed by Sturm et al. (1995), the snow cover in the Snowy Mountains is classified primarily as maritime in areas where there is sufficient accumulation, and as ephemeral at lower elevations and on ablating aspects. Maritime snow is generally deep (>100 cm), with a density >0.30 g cm−3. The snow-ground interface is maintained within 1°C of freezing and relatively high air temperatures promote equitemperature metamorphism throughout the winter. The formation of depth hoar (temperature gradient snow), which is considered to be important in facilitating the development of the subnivean space, does not occur under these conditions. Ephemeral snow is characterized by warm shallow snow that often melts before new snow is deposited. Basal melt is a common feature of snow cover in the Snowy Mountains throughout most of the winter. We reappraise the processes responsible for the formation of the subnivean space under Australian snow conditions and discuss the importance of these processes for understanding the ecology of fauna in the subnivean space. Our findings highlight the value of an explicit description of snow conditions to ecological research in snow-covered areas. As a minimum, researchers should provide a description of basic structural and thermal properties of the snow pack that would allow other researchers to view the work in an appropriate context.

Winter distribution of small mammals in relation to snow cover in the subalpine zone, Australia

AbstractWe present the results of a study that is the first to investigate the landscape‐scale distribution of small mammals in direct relation to the spatial and temporal variation of snow cover. We investigated the distribution of the dusky antechinus Antechinus swainsonii and bush rat Rattus fuscipes in the subalpine zone of Kosciuszko National Park in the Snowy Mountains of south‐eastern Australia. A new hair tube technique was used to detect the presence of small mammals active in the subnivean space. In 2002, we sampled 72 sites stratified by elevation (1501–1600, 1601–1700, 1701–1800 m), aspect (accumulating, ablating) and habitat type (woodland, wet heath, dry heath, grassland). These factors were considered important in influencing snow accumulation and generally reflected the types of habitats available to small mammals. In 2003, the presence of small mammals was investigated at 30 high‐elevation sites including six boulderfields. The development of the subnivean space in the Snowy Mountains is dependent on the presence of structures such as shrubs, boulders and microtopographic features that are capable of supporting a snow layer above ground level. When snow was present, small mammal detections were negatively correlated with snow depth and duration, and positively correlated with the complexity of structures and microtopography. At high elevations detections were largely confined to boulderfields, and at mid and low elevations small mammals were detected primarily in habitats where the subnivean space was most extensive. Antechinus swainsonii and R. fuscipes responded differently to snow cover, with the latter seeming better able to overwinter where snow cover was shallow and patchy, in contrast to A. swainsonii whose occurrence was correlated to the size of the subnivean space.

The implications of snow-based recreation for small mammals in the subnivean space in south-east Australia

The increasing popularity of snow-based recreation activities and the development of ski resorts and associated infrastructure have the potential to affect adversely small mammal fauna that over-winter in the subnivean space. We investigated the effects of human activities on the maintenance of the subnivean space, which is critical to the over-winter survival of small terrestrial mammals in Kosciuszko National Park, south-eastern Australia.The creation of ski pistes, surface ski lifts and over-snow routes involves compression of the snowpack and resulted in small or absent subnivean spaces (average 1.2cm) and high snow cover densities (generally over 0.5gcm−3 and 0.35gcm−3 respectively). By contrast, the subnivean spaces associated with unmodified snow cover averaged 8–20cm depending on vegetation type. The density of unmodified snowpack was less than 0.35gcm−3 in June but increased throughout the season to levels comparable to those of compressed snow. When the snowpack was experimentally compressed at 22 sites, destroying the subnivean space, detections of two small mammal species (Rattus fuscipes and Antechinus swainsonii) significantly (p<0.0001) declined by 75–80%. These species remain active below the snow throughout the winter and depend on the presence of an adequate subnivean space.The removal of vegetation by fire significantly (p<0.0001) reduced the size of the subnivean space regardless of habitat type. Vegetation clearing occurs as part of ground preparation prior to establishing ski runs. Supergrooming, in which surface soil is also disturbed, is likely to have similar (if not more extreme) effects.Nival areas used for snow-based recreation should be managed to minimise negative effects on subnivean fauna, by maintaining natural features associated with subnivean space formation (dense shrubs, boulders and/or microtopography) and confining developments to areas where these features are not present.

Small rodent winter survival: snow conditions limit access to food resources

1. In Fennoscandia during winter small rodents spend most of their time in the subnivean space, between the snow cover and the ground. The subnivean space is probably not a uniform habitat, but broken into accessible and inaccessible patches by ice covering the vegetation. This might reduce access to otherwise available food resources. 2. To test whether ice formations reduce access to food and thus limit winter survival of small rodents, we conducted an experiment where we increased subnivean space by adding corrugated aluminium sheets on the ground before onset of winter. The sheets prevented ice formation, thus mimicking natural occurring subnivean space, and providing more room for animals living in the subnivean space to forage. 3. During the experiment 142 Microtus oeconomus were passive induced transponder (PIT)-tagged, and a system consisting of fixed tube-shaped antennas and PIT-tag readers were used to provide data to analyse winter survival and individual subnivean space use. The extent of winter grazing was measured after snow melt by examining percentage area grazed. 4. The treatment resulted in increased survival which corresponded well with significantly higher space use and more grazing under the sheets. 5. Females showed a positive correlation between probability of survival and body mass while no such effect was observed in males. 6. The results suggest that the snow cover reduces survival in winter by physically enclosing the vegetation in ice and thus reducing access to otherwise available food resources. The amount of ice and its configuration might vary between years due to changing weather patterns. Our results offer a mechanistic explanation for variations in winter survival and suggest incorporating climate variables in future small rodent models. 7. Directional and long-term changes in climate might result in increased ice formation in the subnivean system. Such deterioration may lead to reduced winter survival and act by stabilizing population dynamics and dampening vole cyclicity.

A technique for using hair tubes beneath the snowpack to detect winter-active small mammals in the subnivean space

The study of winter-active small mammals beneath the snowpack has proved challenging for researchers because of the relative inaccessibility. We present a technique using hair tubes that permits the detection of small mammals active in the subnivean space. Hair tubes are cylindrical or funnel-shaped structures containing suitable bait and an adhesive surface that harvests hairs from small mammals as they attempt to reach the bait. Hair tubes eliminate many of the difficulties often associated with live trapping and permit the expansion of systematic sampling to larger scales than allowed by conventional live-trapping methods. The technique was used successfully to detect five small mammal species in the subnivean space in Kosciuszko National Park (KNP) in southeastern Australia. These included the common bush-rat, Rattus fuscipes; the dusky and agile antechinus, Antechinus swainsonii and A. agilis; the broad-toothed rat, Mastacomys fuscus; and the mountain pygmy possum, Burramys parvus. Although hair tubes have a number of limitations, such as not providing a measure of abundance or allowing the identification of individual animals, we believe that these limitations are balanced by the fact that the technique can be used at any spatial scale. Hair tubes are particularly suited to studies of animal distribution at the landscape-scale, because many hair tubes can be deployed and dispersed over large areas, and monitored on a regular basis by a small team of researchers. The technique also makes use of readily available, low-cost materials and could be easily adapted to a range of conditions and different target species.

Habitat Characteristics at Marten Subnivean Access Sites

The occurrence of coarse woody debris (CWD) at sites of subnivean (under snow) access by martens (Martes americana) has not been quantified adequately, and must be better understood to provide suitable winter habitat management for the species. Consequently, we studied subnivean activity of martens in a subalpine forest in southern Wyoming to determine how subnivean space was accessed, and to examine microhabitat characteristics around entry sites. Martens used existing openings in snow, created primarily by logs at low snow depths and by small live spruce and fir trees at greater snow depths

Winter occurrence of the Mountain Pygmy-possum, Burramys parvus (Broom) (Marsupialia: Burramyidae), on Mt Higginbotham, Victoria.

Between June, 1982 and October, 1984 traps were laid in the subnivean space of the optimal breeding habitat of Burramys parvus. Mean trapping success during both the snow-free and post-snow periods was more than 12%. No B. parvus were caught in traps set under the snow; the animals either have long periods of torpor and/or their activity is limited to feeding from their food caches, which are presumably located near to the nest (s). Food caches were similar to those of Burramys in captivity. In only one of 14 buildings located within 100 m of B. parvus habitat on Mt Higginbotham was B. parvus trapped during the snow period. In that building, the University Ski Club Lodge (USCL), where the mean trapping success was 28%, 10 females and 13 males were caught. Most of the females were caught during late October. About 50% of animals had been previously tagged during the snow-free period. During the snow period, the number of adult females moving to the USCL was few (8.1% of previous taggings, compared to adult males, 21%). Males returned to female breeding habitat during the breeding season October-November. These data suggest that the Burramys population is sexually segregated during the nonbreeding season.

COLD-HARDINESS IN THE EGGS OF THE RED TURNIP BEETLE, ENTOMOSCELIS AMERICANA (COLEOPTERA: CHRYSOMELIDAE)

AbstractEggs of the red turnip beetle, Entomoscelis americana Brown, were exposed to temperatures of 0°, −5°, −10°, −15°, and −20°C for 1–8 wk and for 200 days in the laboratory. At −5° and −10°C, there was no death attributable to the cold treatment. At −20°C, the cold treatment caused approximately 15% mortality in the 6- to 8-wk samples and 100% mortality in the 200-day samples. At 0° and −15°C, mortality in the 200-day samples was 39% and 23%, respectively. The data indicate that the embryos of E. americana are able to withstand cold temperatures for long periods and that the optimum temperature range for hibernation (between 0°C and −15°C) is similar to the one this beetle normally experiences in the subnivean air space once the hiemal threshold is established. For Canada, an evaluation of the snow cover and atmospheric air temperature data suggested that egg mortality due to exposure to temperatures of −20°C or lower in the subnivean air space should not occur in the various parts of the red turnip beetle’s range, except possibly the grassland region of the Prairie climatic zone.

Activity of Arthropoda in snow within a coniferous forest, with special reference to Collembola

Winter activity of arthropods from the forest floor were studied in snow and the subnivean space. All but one epedaphic (soil surface dwelling) Collembola species moved up into the snow during winter. Three groups of activity patterns were found. (1) Hypogastrura socialis had a complex behaviour, moving up and down in the snow profile depending on the temperature. It was often found in large numbers on the surface. (2) Other species were occasionally observed on the snow surface, but were usually found in the deeper part of the snow profile. (3) Most epedaphic species were only found in the deeper part of the snow profile. Activity in the snow is assumed to be related to microclimatic conditions occurring mainly in late winter. However, the behaviour pattern is also influenced by the summer ecology of the species.Some collembola and most other arthropods found in the snow were only casual visitors from trees and soil. However, one oribatid species and some predaceous Gamasina mites did also show distinct snow behaviour.