Arctic Rodents Research Articles

Lemming and Vole Cycles: A New Intrinsic Model.

It is 100 years since the first paper described the multiannual cycles in Arctic rodents and lagomorphs. The mechanisms driving population cycles in animals like lemmings and voles are complex, often attributed to extrinsic factors, such as food availability and quality, pathogens, parasites and/or predators. While extrinsic factors provide insights into population cycles, none fully explain the phenomenon. We propose an underlying innate, intrinsic mechanism, based on epigenetic regulation, that drives population cycles under harsh arctic conditions. We propose that epigenetically driven phenotypic changes associated with sexual development, growth and behaviour accumulate over time in offspring, eventually producing a phase change from rising population density to eventual population collapse. Under this hypothesis, and unlike previous hypotheses, extrinsic factors modify population cycles but would not be primary drivers. The interaction between our intrinsic cycle and extrinsic factors explains established phenomena like delayed-density dependence, whereby population growth is controlled by time-dependent negative feedback. We advocate integrating a century of field research with the latest epigenetic analysis to better understand the drivers of population cycles.

Snow hardness impacts intranivean locomotion of arctic small mammals

AbstractFossorial locomotion is often considered as the most energetically costly of all terrestrial locomotion. Small arctic rodents, such as lemmings, dig tunnels not only in the soil but also through the snowpack, which is present for over 8 months of the year. Lemmings typically dig in the softest snow layer called the depth hoar but with climate change, melt‐freeze and rain‐on‐snow (ROS) events are expected to increase in the Arctic, leading to a higher frequency of hardened snowpacks. We assessed the impacts of snow hardness on the locomotion of two lemming species showing different morphological adaptations for digging. We hypothesized that an increase in snow hardness would (1) decrease lemming performance and (2) increase their effort while digging, but those responses would differ between lemming species. We exposed four brown lemmings (Lemmus trimucronatus) and three collared lemmings (Dicrostonyx groenlandicus) to snow of different hardness (soft, hard, and ROS) during 30‐min trials (n = 63 trials) in a cold room and filmed their behavior. We found that the digging speed and tunnel length of both species decreased with snow hardness and density, underlining the critical role of snow properties in affecting lemming digging performance. During the ROS trials, time spent digging by lemmings increased considerably and they also started using their incisors to help break the hard snow, validating our second hypothesis. Overall, digging performance was higher in collared lemmings, the species showing more morphological adaptations to digging, than in brown lemmings. We conclude that the digging performance of lemming is highly dependent on snowpack hardness and that the anticipated increase in ROS events may pose a critical energetic challenge for arctic rodent populations.

Long-term monitoring reveals topographical features and vegetation that explain winter habitat use of an Arctic rodent

The quality of wintering habitats, such as depth of snow cover, plays a key role in sustaining population dynamics of Arctic lemmings. However, few studies so far investigated habitat use during the Arctic winter. Here, we used a unique long-term time series to test whether lemmings are associated with topographical and vegetational habitat features for their wintering sites. We examined yearly numbers and distribution of 22 769 winter nests of the collared lemming Dicrostonyx groenlandicus (Traill, 1823) from an ongoing long-term research on Traill Island, Northeast Greenland, collected between 1989 and 2019, and correlated this information with data on dominant vegetation types, elevation, and slope. We found that the number of lemming nests was highest in areas with a high proportion of Dryas heath, but was also correlated with other vegetation types, suggesting some flexibility in resource use of wintering lemmings. Furthermore, lemmings showed a higher use for sloped terrain, probably as it enhances the formation of deep snow drifts, which increases the insulative characteristics of the snowpack and protection from predators. With global warming, prime lemming winter habitats may become scarce through alteration of snow physical properties, potentially resulting in negative consequence for the whole community of terrestrial vertebrates.

Incisor microwear of Arctic rodents as a proxy for microhabitat preference

Changing environmental conditions in the Arctic make it important to document and understand habitat preferences and flexibility of vulnerable high-latitude mammals. Indirect proxies are especially useful for elusive species, such as rodents. This study explores incisor microwear as an indicator of variation in behavior and microhabitat use in Siberian lemmings (Lemmus sibiricus) and narrow-headed voles (Lasiopodomys gregalis) from the Yamal Peninsula, Russia. Fifty-nine individuals were sampled at four sites along a latitudinal gradient from forest-tundra ecotone to high-Arctic tundra. Lemmings are present at the northernmost site, voles at the southernmost site, and both species at the middle two. Lemmus sibiricus prefers wet, mossy lowland, whereas La. gregalis favors drier thickets and more open microhabitats and burrows underground. Feature-based analyses indicate higher densities of features and more uniformly oriented striations for voles than lemmings at sites with both species. The species also differ significantly in microwear texture attributes suggesting larger features for lemmings, and smaller ones, but more of them, for voles. While no texture differences were found between sites within species, voles from sites with open tundra have higher striation densities than those from the forest-tundra ecotone. Furthermore, lemmings from open tundra sites have higher striation densities than those from the water-saturated, moss-covered northernmost site. While microhabitat preferences and burrowing by voles likely contribute to differences between species, variation within seems to reflect habitat variation given differences in abrasive loads between sites. This suggests that incisor microwear patterning can be used to track microhabitat differences among Arctic rodent populations.

Snow physical properties may be a significant determinant of lemming population dynamics in the high Arctic

Cyclic population fluctuations are common in boreal and Arctic species but the causes of these cycles are still debated today. Among these species, lemmings are Arctic rodents that live and reproduce under the snow and whose large cyclical population fluctuations in the high Arctic impact the whole tundra food web. We explore, using lemming population data and snow modeling, whether the hardness of the basal layer of the snowpack, determined by rain-on-snow events (ROS) and wind storms in autumn, can affect brown lemming population dynamics in the Canadian high Arctic. Using a 7-year dataset collected on Bylot Island, Nunavut, Canada over the period 2003–2014, we demonstrate that liquid water input to snow is strongly inversely related with winter population growth (R2 ≥ 0.62) and to a lesser extent to lemming summer densities and winter nest densities (R2 = 0.29–0.39). ROS in autumn can therefore influence the amplitude of brown lemming population fluctuations. Increase in ROS events with climate warming should strongly impact the populations of lemmings and consequently those of the many predators that depend upon them. Snow conditions may be a key factor influencing the cyclic dynamics of Arctic animal populations.

Spatial distribution in Norwegian lemming Lemmus lemmus in relation to the phase of the cycle

Competition between individuals of the same or different species affects spatial distribution of organisms at any given time. Consequently, a species geographical distribution is related to population dynamics through density-dependent processes. Small Arctic rodents are important prey species in many Arctic ecosystems. They commonly show large cyclic fluctuations in abundance offering a potential to investigate how landscape characteristics relates to density-dependent habitat selection. Based on long-term summer trapping data of the Norwegian lemming (Lemmus lemmus) in the Scandinavian Mountain tundra, we applied species distribution modeling to test if the effect of environmental variables on lemming distribution changed in relation to the lemming cycle. Lemmings were less habitat specific during the peak phase, as their distribution was only related to primary productivity. During the increase phase, however, lemming distribution was, in addition, associated with landscape characteristics such as hilly terrain and slopes that are less likely to get flooded. Lemming habitat use varied during the cycle, suggesting density-dependent changes in habitat selection that could be explained by intraspecific competition. We believe that the distribution patterns observed during the increase phase show a stronger ecological signal for habitat preference and that the less specific habitat use during the peak phase is a result of lemmings grazing themselves out of the best habitat as the population grows. Future research on lemming winter distribution would make it possible to investigate the year around strategies of habitat selection in lemmings and a better understanding of a fundamental actor in many Arctic ecosystems.

Landscapes of fear or competition? Predation did not alter habitat choice by Arctic rodents

In systems where predation plays a key role in the dynamics of prey populations, such as in Arctic rodents, it is reasonable to assume that differential patterns of habitat use by prey species represent adaptive responses to spatial variation in predation. However, habitat selection by collared (Dicrostonyx groenlandicus) and brown (Lemmus trimucronatus) lemmings depends on intra- and inter-specific densities, and there has been little agreement on the respective influences of food abundance, predators, and competition for habitat on lemming dynamics. Thus, we investigated whether predation affected selection of sedge-meadow versus upland tundra by collared lemmings in the central Canadian Arctic. We first controlled for the effects of competition on lemming habitat selection. We then searched for an additional signal of predation by comparing habitat selection patterns between 12 control plots and one large grid where lemmings were protected from predators by fencing in 1996 and 1997, but not during 5 subsequent years when we monitored habitat use in the grid as well as in the control plots. Dicrostonyx used upland preferentially over meadows and was more numerous in 1996 and 2011 than in other sample years. Lemmus was also more abundant in 1996 than in subsequent years, but its abundance was too low in the exclosure to assess whether exclusion of predators influenced its habitat selection. Contrary to the effects of competition, predation had a negligible impact on the spatial dynamics of Dicrostonyx, at least during summer. These results suggest that any differences in predation risk between the two habitats have little direct influence on the temporal dynamics of Dicrostonyx even if induced through predator-prey cycles.

The Red Knot (Calidris canutus rufa) decline in the western hemisphere: is there a lemming connection?

Numbers of Western Atlantic Red Knots (Calidris canutus rufa (A. Wilson, 1813)) have declined since 1980, with a sustained downward trend observed after 1998. Because the reproductive output of a closely related Eurasian subspecies (Calidris canutus islandica (L., 1767)) is known to be low when lemming numbers are low, and because lemming cycles in Fennoscandia were recently interrupted, we investigated the relationship between the rodent cycle in arctic Canada and numbers of C. c. rufa migrating through the United States. Shooting records from Cape Cod in the 1800s and Red Knot counts on the Delaware Bay from 1986 to 1998 cycled with 4-year periods. Annual peaks in numbers of Red Knots stopping in the Delaware Bay in 1986–1998 occurred 2 years after arctic rodent peaks more often than expected at random. The results suggest that the reproductive output of C. c. rufa was linked to the rodent cycle before the Red Knot decline. There is no evidence that such a link existed after 1998. These findings are consistent with the hypothesis that an interruption of the rodent cycle in Red Knot habitat could have been a driver in the recent Red Knot decline. Field studies in the Arctic are needed to further investigate this hypothesis.

Habitat change and the scale of habitat selection: shifting gradients used by coexisting Arctic rodents

The conservation and understanding of biodiversity requires development and testing of models that illustrate how climate change and other anthropogenic effects alter habitat and its selection at different spatial scales. Models of fitness along a habitat gradient illustrate the connection between fine‐scale variation in fitness and the selection of habitat as discontinuous patches in the landscape. According to these models, climate change can increase fitness values of static habitats, shift the fitness value of habitat patches along underlying gradients of habitat quality, or alter both fitness and habitat quality. It should be possible to differentiate amongst these scenarios by associating differences in the abundance and distribution of species with metrics of habitat that document the gradient while controlling for changes in density at larger scales of analysis. Comparisons of habitat selection by two species of lemmings, over an interval of 15 years, are consistent with the theory. The pattern of habitat selection at the scale of wet versus dry tundra habitats changed through time. The change in habitat selection was reflected by different, but nevertheless density‐dependent, patterns of association with the structure and composition of habitat. Abundant collared lemmings abandoned stations where altered habitat characteristics caused a shift to new locations along the wet‐to‐dry gradient. The confirmation of scale‐dependent theory provides new insights into how one might begin to forecast future habitat selection under different scenarios of climate and habitat change.

Habitat selection and the scale of ghostly coexistence among Arctic rodents

Competition between coexisting species existing near their stable equilibrium can be obscured if they occupy separate habitats. Theories of habitat selection promise an ability to reveal the underlying ghost of competition by using isodars to infer the behavioural map of habitat selection. We tested the theory with two years of data on abundance and habitat preference by three Arctic rodent species living at low density along a gradient of wet to dry tundra on Herschel Island in Canada's western Arctic. Generalist brown lemmings exhibited a constant partial preference toward wet tundra whereas specialist collared lemmings and voles occupied the driest and wettest zones respectively. Although both lemming species compete for habitats elsewhere in the Canadian Arctic, isodar analyses suggest that the three species occupy wet and dry habitats independently of one another on Herschel Island. Competition at this large scale may be hidden at low densities, however, if the wet‐dry dichotomy is too coarse. Analyses at a finer subdivision of habitat revealed that these species coexist by using different microhabitats. Collared lemmings shifted their niche towards even drier habitat as the abundance of brown lemmings increased. We were thus able to reveal the ghost of competition lurking at large scales through a more refined analysis at smaller scales of density‐dependent habitat use.

Forecasting ecological and evolutionary strategies to global change: an example from habitat selection by lemmings

Ecologists and evolutionary biologists must develop theories that can predict the consequences of global warming and other impacts on Earth's biota. Theories of adaptive habitat selection are particularly promising because they link distribution and density with fitness. The evolutionarily stable strategy that emerges from adaptive habitat choice is given by the system's habitat isodar, the graph of densities in pairs of habitats such that the expectation of fitness is the same in each. We illustrate how isodars can be converted into adaptive landscapes of habitat selection that display the density- and frequency-dependent fitness of competing strategies of habitat use. The adaptive landscape varies with the abundance of habitats and can thus be used to predict future adaptive distributions of individuals under competing scenarios of habitat change. Application of the theory to three species of Arctic rodents living on Herschel Island in the Beaufort Sea predicts changes in selection gradients as xeric upland increases in frequency with global warming. Selection gradients will become more shallow for brown lemming (Lemmus trimucronatus) and tundra vole (Microtus oeconomus) strategies that preferentially exploit mesic habitat. Climate change will cause selection gradients for the alternative strategy of using mostly xeric habitat to become much steeper. Meanwhile, the adaptive landscape for collared lemmings (Dicrostonyx groenlandicus), which specialize on xeric Dryas-covered upland, will become increasingly convex. Changes in the adaptive landscapes thus predict expanding niches for Lemmus and Microtus, and a narrower niche for Dicrostonyx. The ability to draw adaptive landscapes from current patterns of distribution represents one of the few methods available to forecast the consequences of climate change on the future distribution and evolution of affected species.

Influence of Climate Warming on Arctic Mammals? New Insights from Ancient DNA Studies of the Collared Lemming Dicrostonyx torquatus

BackgroundGlobal temperature increased by approximately half a degree (Celsius) within the last 150 years. Even this moderate warming had major impacts on Earth's ecological and biological systems, especially in the Arctic where the magnitude of abiotic changes even exceeds those in temperate and tropical biomes. Therefore, understanding the biological consequences of climate change on high latitudes is of critical importance for future conservation of the species living in this habitat. The past 25,000 years can be used as a model for such changes, as they were marked by prominent climatic changes that influenced geographical distribution, demographic history and pattern of genetic variation of many extant species. We sequenced ancient and modern DNA of the collared lemming (Dicrostonyx torquatus), which is a key species of the arctic biota, from a single site (Pymva Shor, Northern Pre Urals, Russia) to see if climate warming events after the Last Glacial Maximum had detectable effects on the genetic variation of this arctic rodent species, which is strongly associated with a cold and dry climate.ResultsUsing three dimensional network reconstructions we found a dramatic decline in genetic diversity following the LGM. Model-based approaches such as Approximate Bayesian Computation and Markov Chain Monte Carlo based Bayesian inference show that there is evidence for a population decline in the collared lemming following the LGM, with the population size dropping to a minimum during the Greenland Interstadial 1 (Bølling/Allerød) warming phase at 14.5 kyrs BP.ConclusionOur results show that previous climate warming events had a strong influence on genetic diversity and population size of collared lemmings. Due to its already severely compromised genetic diversity a similar population reduction as a result of the predicted future climate change could completely abolish the remaining genetic diversity in this population. Local population extinctions of collared lemmings would have severe effects on the arctic ecosystem, as collared lemmings are a key species in the trophic interactions and ecosystem processes in the Arctic.

The Late Pleistocene and Holocene rodents of the Pre-Urals subarctic

In this paper we present a revision and review of the available palaeofaunal data on Late Pleistocene and Holocene rodents of the subarctic sector adjacent to the Urals, in order to describe the dynamic changes of the rodent fauna. Our main goal was to classify the examined communities in terms of their zonal characteristics. It was shown that the most important changes in the fauna composition and structure occurred ca. 8000–9000 years ago; at that time the arctic rodent complex of the Pleistocene (which included only 3 species) was superseded by that of the forest-tundra type. The latter was composed of 10 species, many of which typical of forest associations. The process of the biota development in the region was strongly affected by the early and extremely abrupt arrival of the Holocene optimum first stage. Later on in the Holocene, the tundra elements increased their role again, but within the same forest-tundra type. Specially discussed are problems with the recent sub-species of the narrow-skulled vole and the collared lemming, and the history of their development.

Responses of Arctic Rodent Populations to Nutritional Factors

All arctic rodents are primarily herbivorous, but their population dynamics vary from relative stability to oscillatory instability. Loop analyses for models of an oscillatory population (brown lemmings) and a stable population (arctic ground squirrels) suggest that strong self-regulation produces stability but that strong interactions between herbivores and plant (forage) quality do not. Strong interaction with positive factors (plant nutrients) produces simple instability, and strong interaction with negative factors (plant secondary compounds) produces oscillations. Because forage quality is determined by herbivore response as well as by plant characteristics, it can only be assessed by feeding trials. As a result, there are few empirical studies that adequately treat the influence of forage quality on herbivore populations. Nevertheless, a review of available information suggests that the relative availability of high quality forage can account for differences in densities of arctic rodents between habitats and seasons. The role of forage quality in cyclic changes of density is not as clear; population trends do not seem simply to follow nutrient concentrations in forage, but they may be linked to fluctuations in plant secondary compounds.

Quantitative morphology and environmental responses of the pineal gland in the collared lemming (Dicrostonyx groenlandicus).

Collared lemmings from Churchill, Manitoba, and their descendants were studied in captivity to define neuroendocrine and related histophsiological characteristics and responses, particularly in relation to photic and temperature conditions. Relatively great pineal size (0.1755 +/- 0.0167 mm3, or 3.08 +/- 0.30 = pineal volume in mm3 X 10(3)/body weight in gm; N = 16) shown in this arctic rodent is consistent with the suggestion that pineal size and significance may tend to be greater in more northern (higher latitude) species. Total number of nucleated cells per pineal averaged 137,000 +/- 10,500. Pinealocytes (105,000 +/- 8,700/pineal) and other cell types were present in relative numbers typical of mammalian pineal glands, and were not numerically correlated with age, sex, or location or circumstances of birth and early postnatal life. Chronic exposure to warmer (21-27 degrees C) in comparison with colder (-9 to -6 degrees C) environments, whatever the illumination, led to greater pinealocyte activity, as shown especially by nucleolar diameter, throughout most of the nine regions of the organ analyzed cytologically (all regions combined: P less than 0.001). Increased pinealocyte activity in chronic darkness was suggested by similar evidence (P less than 0.01), but in comparison with the thermal effects, was less marked and more variable in different regions of the organ. These and other findings of this study indicate that the Dicrostonyx pineal organ is morphologically unique, relatively large in size, and cytologically responsive to environmental conditions.

Cold acclimation in arctic lemmings

Abstract o 1. The lemmings, Arctic rodents, show cold acclimation as measured by a number of variables: food and water consumption, liver temperature, and organ weights. 2. Cold acclimation of lemmings is apparently more rapid than that of temperate mammals. 3. The rapid cold acclimation in lemmings supports the hypothesis that compensation of a number of physiological variables is essentially complete within the first week of cold exposure as opposed to requiring months.

Circadian variations in adrenal secretion of lemmings, voles and mice.

ABSTRACT Daily variations in adrenal secretion by glands from arctic rodents were measured in vitro. Serial-sacrifice, short-term incubation studies yield similar results to those data obtained through organ-culture methods. Adrenal secretory rates display some desynchronization from locomotor activity during the summer solstice, although circadian variation persists during all seasons of the arctic year.

The Pancreatic Islets of Desert Rodents

During a recent study of the endocrine organs of the collared lemming, Dicrostonyx, a relatively low pancreatic alpha: beta cell ratio was noted in this arctic rodent. It was discovered also that comparative data on the pancreatic islets of rodents in the literature are extremely meager. It seems likely that in at least some species, modifications or specializations in carbohydrate metabolism or utilization associated with climatic adaptations, may be related to modifications in the endocrine glands, especially the pancreatic islets. A survey of the microanatomy of the islets in some North American desert rodents reported here tends to support this belief and contributes data on trends within the Heteromyidae. I am grateful to John Eisenberg, Dennis Galloway, Richard Graham, John Pun, Mary Taylor, and Alan Ziegler for assistance during the procurement of specimens and to Dr. Seth Benson for aid in the identification of the specimens of Perognathus.