Lemming Cycle Research Articles

Population regulation and limitation-insights from lemming cycles: past, present and future.

Population regulation and limitation-insights from lemming cycles: past, present and future.

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.

Taking the beat of the Arctic: are lemming population cycles changing due to winter climate?

Reports of fading vole and lemming population cycles and persisting low populations in some parts of the Arctic have raised concerns about the spread of these fundamental changes to tundra food web dynamics. By compiling 24 unique time series of lemming population fluctuations across the circumpolar region, we show that virtually all populations displayed alternating periods of cyclic/non-cyclic fluctuations over the past four decades. Cyclic patterns were detected 55% of the time (n = 649 years pooled across sites) with a median periodicity of 3.7 years, and non-cyclic periods were not more frequent in recent years. Overall, there was an indication for a negative effect of warm spells occurring during the snow onset period of the preceding year on lemming abundance. However, winter duration or early winter climatic conditions did not differ on average between cyclic and non-cyclic periods. Analysis of the time series shows that there is presently no Arctic-wide collapse of lemming cycles, even though cycles have been sporadic at most sites during the last decades. Although non-stationary dynamics appears a common feature of lemming populations also in the past, continued warming in early winter may decrease the frequency of periodic irruptions with negative consequences for tundra ecosystems.

A beacon of dung: using lemming (Lemmus lemmus) winter nests and DNA analysis of faeces to further understand predator\u2013prey dynamics in Northern Sweden

The hypothesis that predation is the cause of the regular small rodent population oscillations observed in boreal and Arctic regions has long been debated. Within this hypothesis, it is proposed that the most likely predators to cause these destabilizing effects are sedentary specialists, with small mustelids being possible candidates. One such case would be the highly specialized least weasel (Mustela nivalis) driving the Norwegian lemming (Lemmus lemmus) cycle in Fennoscandia. These predators are often elusive and therefore distribution data can only be based on field signs, which is problematic when various mustelid species are sympatric, such as weasels and stoats (Mustela erminea). Here we present the results of using mustelid faeces in predated winter lemming nests to correctly identify the predator and thus discern which species exerts the strongest predation pressure on lemming winter populations. Samples were obtained during different phases in the lemming cycle, spanning 6 years, to account for different prey densities. Faecal mitochondrial DNA extraction and amplification of a 400-bp fragment was successful in 92/114 samples (81%); the sequencing of these samples proved that most predation occurrences (83%) could be attributed to the least weasel. These findings support the hypothesis that weasels in particular show high specificity in predation and could therefore be candidates to driving the lemming cycle in this area. We conclude that DNA analysis of faecal remains around predated nests can be a useful tool for further investigations concerning predator–prey interactions in the tundra.

Arctic fox winter dietary response to damped lemming cycles estimated from fecal DNA

Abstract Climate-caused changes in prey abundance may alter predator–prey dynamics in the Arctic food web. Lemmings (Dicrostonyx spp.) are important prey for Arctic foxes (Vulpes lagopus) and their annual population fluctuations drive fox reproduction, creating strongly linked predator–prey population cycles. Winter diet directly impacts Arctic fox reproductive success, but winter prey diversity on the tundra is low. Strategies such as using the marine environment to scavenge seals have allowed Arctic foxes to persist during years of low lemming abundance. However, warming winters have decreased snowpack quality, preventing lemmings from reaching their previous high abundances, which may reduce their impact on predator dynamics. We investigated Arctic fox dietary response to lemming abundance by reconstructing Arctic fox winter diet in the low Arctic. Next-generation sequencing of fecal DNA, from samples (n = 627) collected at dens in winters of 2011–2018, identified prey both from terrestrial and marine environments. Despite lemming cycle damping, Arctic foxes still increased lemming consumption during years of higher lemming abundance. Alternative prey such as marine resources were consumed more during years of low lemming abundance, with up to 45% of samples containing marine resources in low lemming years. In addition, Arctic foxes consumed high proportions of meadow voles (Microtus pennsylvanicus), which may represent a new alternative prey, suggesting climate change may be creating new foraging opportunities. Changes in prey abundance illustrate how climate-caused disturbances are altering Arctic food-web dynamics. Dietary flexibility and availability of alternative prey may become increasingly important for Arctic predators as the Arctic continues to change.

The Arctic fox (Vulpes lagopus L.) on the Kola Peninsula (Russia): silently disappearing in the mist of data deficiency?

The Arctic fox (Vulpes lagopus L.) population on the Kola Peninsula occupies an intermediate, and potentially connecting, position between foxes living on the Scandinavian Peninsula and populations further east in Russia, but very little is known about the status of this population. Here we summarize data from the literature, forgotten archival sources about research in the first half of the twentieth century, and the results of several independent expeditions undertaken over the past two decades. These materials include data on fur harvesting, incomplete monitoring data from official winter track counts of game animals, local knowledge, and our own observations. Our research revealed the extremely poor state of the Arctic fox population on the Kola Peninsula. According to our estimates, the current population is likely isolated and consists of no more than a few dozen adults. The fur return data, together with long-term data on small rodent abundance, suggest that irregular and fading out lemming cycles were a major driver of the Arctic fox population decline. The thorough research from the 1930s contrasts strongly with the lack of interest in studying and monitoring the population in recent decades, which is not even listed as a threatened species in the regional Red Data Book. In fact, the work performed here filled a more than a half-century gap in the study of the population and allowed us to determine the urgent need to resume research and immediately take active measures to protect and promote the recovery of the species in the region.

Relating the 4-year lemming (Lemmusspp. andDicrostonyxspp.) population cycle to a 3.8-year lunar cycle and ENSO

Reported peak years of lemming (Lemmus spp. and Dicrostonyx spp.) and Arctic fox (Vulpes lagopus (Linnaeus, 1758)) abundance were compiled from the literature for 12 locations spanning 127 years. The mean period of the 34 reported lemming and Arctic fox cycles from 1868 to 1994 was 3.8 years, suggesting that the period of the 4-year cycle is actually 3.8 years. Peak population years were predicted using a simple model based on a 3.8-year lunar cycle. For nearly 130 years, reported years of peak abundance of lemmings and Arctic foxes were significantly correlated with and have persistently stayed in phase with predicted peak years of abundance. Over the same period, predicted peak years of lemming abundance have been closely aligned with peak (i.e., La Niña) years of the January–March Southern Oscillation Index (SOI). From 1952 to 1995, peak flowering in Norway tended to occur close to trough June–August SOI (El Niño) years. The hypothesis proposed is that the 3.8-year lunar cycle governs the timing of the lemming cycle, but it does not cause the population cycling itself. If this hypothesis is true, then the heretofore unexplained source of the persistent periodicity and quasi-metronomic regularity of the lemming cycle is identified.

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.

Vole abundance and reindeer carcasses determine breeding activity of Arctic foxes in low Arctic Yamal, Russia

BackgroundHigh latitude ecosystems are at present changing rapidly under the influence of climate warming, and specialized Arctic species at the southern margin of the Arctic may be particularly affected. The Arctic fox (Vulpes lagopus), a small mammalian predator endemic to northern tundra areas, is able to exploit different resources in the context of varying tundra ecosystems. Although generally widespread, it is critically endangered in subarctic Fennoscandia, where a fading out of the characteristic lemming cycles and competition with abundant red foxes have been identified as main threats. We studied an Arctic fox population at the Erkuta Tundra Monitoring site in low Arctic Yamal (Russia) during 10 years in order to determine which resources support the breeding activity in this population. In the study area, lemmings have been rare during the last 15 years and red foxes are nearly absent, creating an interesting contrast to the situation in Fennoscandia.ResultsArctic fox was breeding in nine of the 10 years of the study. The number of active dens was on average 2.6 (range 0–6) per 100 km2 and increased with small rodent abundance. It was also higher after winters with many reindeer carcasses, which occurred when mortality was unusually high due to icy pastures following rain-on-snow events. Average litter size was 5.2 (SD = 2.1). Scat dissection suggested that small rodents (mostly Microtus spp.) were the most important prey category. Prey remains observed at dens show that birds, notably waterfowl, were also an important resource in summer.ConclusionsThe Arctic fox in southern Yamal, which is part of a species-rich low Arctic food web, seems at present able to cope with a state shift of the small rodent community from high amplitude cyclicity with lemming dominated peaks, to a vole community with low amplitude fluctuations. The estimated breeding parameters characterized the population as intermediate between the lemming fox and the coastal fox ecotype. Only continued ecosystem-based monitoring will reveal their fate in a changing tundra ecosystem.

Ecosystem drivers of an Arctic fox population at the western fringe of the Eurasian Arctic

ABSTRACTThe distribution of traditional breeding dens on the Varanger Peninsula (70–71°N) in northernmost Fennoscandia indicates that this area once harboured a large Arctic fox population. Early 20th century naturalists regarded the coastal tundra of the Fennoscandian Low Arctic to be a stronghold for the species. At the start of our research in 2004, however, the local Arctic fox population was critically small and most neighbouring populations had been extirpated. Here, we synthesize the results of 11 years of research to highlight ecosystem drivers behind the critical state of the Arctic fox in Low-Arctic Fennoscandia. We identify two fundamental drivers: (1) an increasingly climate-driven irregularity of the lemming cycle and (2) a management- and climate-driven increase in the abundance of red fox that is subsidized by more ungulate carrion. Arctic fox reproductive success is low when lemmings are scarce (despite high vole abundance), while red foxes exclude Arctic foxes from high-quality breeding t...

Ilkka Hanski and Small Mammals: from Shrew Metapopulations to Vole and Lemming Cycles

Ilkka Hanski may be best known for his work on insect and metapopulation dynamics, but he also contributed significantly to small mammal research. In the early 1980s he became interested in shrew dynamics, energetics, and of course, shrew metapopulations. He aimed at understanding the population biological consequences of body size in different shrew species. Feeding habits and environmental stochasticity affect shrew species in profoundly different ways: due to their short survival time small species have high extinction rates but their dispersal and colonization capacity is high which enables them to survive as metapopulations. After Hansson and Henttonen reported the Fennoscandian gradients in vole dynamics in the mid-1980s, Hanski became interested in vole and lemming cycles. The first models on this were published with Henttonen and Hansson in 1991 where the roles of specialist and generalist predators were assessed. Later, the models were further developed with Korpimaki and Turchin, with model para...

Not only mosses: lemming winter diets as described by DNA metabarcoding

The temporal dynamics of most tundra food webs are shaped by the cyclic population dynamics of lemmings. While processes during winter may be behind the recent disruptions of lemming cycles, lemming winter ecology is poorly known. We present here the first DNA metabarcoding data on the winter diet of Norwegian lemmings (Lemmus lemmus), based on feces collected after a winter of population increase. Prostrate willows, mosses, and graminoids dominated the species winter diet, indicating that the conventional idea of lemmings as moss-specialists should be revised. The behavior of lemming-plant models in theoretical studies is conditional on the assumptions of mosses being their main winter food item. As shrubs have been excluded from the framework of these models, incorporating them in future modeling studies should nuance our understanding on how plants affect lemmings. We also sampled diet of a few individuals found dead on top of the snow. These individuals had relatively empty stomachs and had, prior to death, relied heavily on mosses. This apparent lack of abundant good quality indicates spatial heterogeneity in local food availability during the population increase phase.

Timing of population peaks of Norway lemming in relation to atmospheric pressure: A hypothesis to explain the spatial synchrony.

Herbivore cycles are often synchronized over larger areas than what could be explained by dispersal. In Norway, the 3–4 year lemming cycle usually show no more than a one-year time lag between different regions, despite distances of up to 1000 km. If important food plants are forced to reallocate defensive proteins in years with high seed production, spatially synchronized herbivore outbreaks may be due to climate-synchronized peaks in flowering. Because lemming peaks are expected to occur one year after a flowering peak, and the formation of flower buds is induced in the year before flowering, a two-year time lag between flower-inducing climate events and lemming peaks is predicted. At Hardangervidda, South Norway, the probability that a year was a population peak year of lemming during 1920–2014 increased with increasing midsummer atmospheric pressure two years earlier, even when the number of years since the previous peak was accounted for.

Breeding in a den of thieves: pros and cons of nesting close to egg predators

AbstractBreeding success of many Arctic‐breeding bird populations varies with lemming cycles due to prey switching behavior of generalist predators. Several bird species breed on islands to escape from generalist predators like Arctic fox Vulpes lagopus, but little is known about how these species interact. We studied brent geese Branta bernicla bernicla that share islands with gulls (Larus spec.) in Taimyr, Siberia (Russia). On one hand, gulls are egg predators, which occasionally steal an egg when incubating geese leave the nest for foraging bouts. On the other hand, gulls import marine resources to the islands, enriching the soil with their guano. We considered three hypotheses regarding clutch size of brent geese after partial nest predation. According to the “predator proximity hypothesis”, clutch size is expected to be smallest close to gulls, because of enhanced predator exposure. Conversely, clutch size is expected to be largest close to gulls, because of the supposedly better feeding conditions close to gulls, which might reduce nest recess times of geese and hence egg predation risk (“guano hypothesis”). Furthermore, gulls may defend their nesting territory, and thus nearby goose nests might benefit from this protection against other gulls (“nest association hypothesis”). We mapped goose and gull nests toward the end of the goose incubation period. In accordance with the latter two hypotheses, goose clutch size decreased with distance to the nearest gull nest in all but the lemming peak year. In the lemming peak year, clutch size was consistently high, indicating that partial nest predation was nearly absent. By mapping food quantity and quality, we found that nitrogen availability was indeed higher closer to gull nests, reflecting guanofication. Unlike predicted by the nest association hypothesis, a predation pressure experiment revealed that egg predation rate decreased with distance to the focal gull nests. We therefore propose that higher food availability close to gulls enables female geese to reduce nest recess time, limiting egg predation by gulls.

Loss of periodicity in breeding success of waders links to changes in lemming cycles in Arctic ecosystems

Lemming population cycles in the Arctic have an important impact on the Arctic food web, indirectly also affecting breeding success in Arctic‐nesting birds through shared predators. Over the last two decades lemming cycles have changed in amplitude and even disappeared in parts of the Arctic. To examine the large scale effect of these recent changes we re‐analysed published data from the East Atlantic Flyway (EAF), where a relationship between lemming cycles and wader breeding success was earlier found, and new data on breeding success of waders in the East Asian–Australasian Flyway (EAAF).We found that 1) any long‐term periodicities in wader breeding success existed only until the year 2000 in the EAAF and until the 1980s in the EAF; 2) studying these patterns at a smaller spatial scale, where the Siberian–Alaskan breeding grounds were divided into five geographical units largely based on landscape features, breeding success of waders from the EAAF was not correlated to an index of predation pressure, but positively correlated to Arctic summer temperatures in some species. We argue that fading out of lemming cycles in some parts of the Arctic is responsible for faltering periodicity in wader breeding success along both flyways. These changed conditions have not yet resulted in any marked changing trends in breeding success across years, and declining numbers of waders along the EAAF are therefore more likely a result of changing conditions at stop‐over and wintering sites.

The influence of weather and lemmings on spatiotemporal variation in the abundance of multiple avian guilds in the arctic.

Climate change is occurring more rapidly in the Arctic than other places in the world, which is likely to alter the distribution and abundance of migratory birds breeding there. A warming climate can provide benefits to birds by decreasing spring snow cover, but increases in the frequency of summer rainstorms, another product of climate change, may reduce foraging opportunities for insectivorous birds. Cyclic lemming populations in the Arctic also influence bird abundance because Arctic foxes begin consuming bird eggs when lemmings decline. The complex interaction between summer temperature, precipitation, and the lemming cycle hinder our ability to predict how Arctic-breeding birds will respond to climate change. The main objective of this study was to investigate the relationship between annual variation in weather, spring snow cover, lemming abundance and spatiotemporal variation in the abundance of multiple avian guilds in a tundra ecosystem in central Nunavut, Canada: songbirds, shorebirds, gulls, loons, and geese. We spatially stratified our study area based on vegetation productivity, terrain ruggedness, and freshwater abundance, and conducted distance sampling to estimate strata-specific densities of each guild during the summers of 2010–2012. We also monitored temperature, rainfall, spring snow cover, and lemming abundance each year. Spatial variation in bird abundance matched what was expected based on previous ecological knowledge, but weather and lemming abundance also significantly influenced the abundance of some guilds. In particular, songbirds were less abundant during the cool, wet summer with moderate snow cover, and shorebirds and gulls declined with lemming abundance. The abundance of geese did not vary over time, possibly because benefits created by moderate spring snow cover were offset by increased fox predation when lemmings were scarce. Our study provides an example of a simple way to monitor the correlation between weather, spring snow cover, lemming abundance, and spatiotemporal variations in Arctic-breeding birds.

Faltering lemming cycles reduce productivity and population size of a migratory Arctic goose species

1. The huge changes in population sizes of Arctic-nesting geese offer a great opportunity to study population limitation in migratory animals. In geese, population limitation seems to have shifted from wintering to summering grounds. There, in the Arctic, climate is rapidly changing, and this may impact reproductive performance, and perhaps population size of geese, both directly (e.g. by changes in snow melt) or indirectly (e.g. by changes in trophic interactions).2. Dark-bellied brent geese (Branta bernicla bernicla L.) increased 20-fold since the 1950s. Its reproduction fluctuates strongly in concert with the 3-year lemming cycle. An earlier analysis, covering the growth period until 1988, did not find evidence for density dependence, but thereafter the population levelled off and even decreased. The question is whether this is caused by changes in lemming cycles, population density or other factors like carry-over effects.3. Breeding success was derived from proportions of juveniles. We used an information-theoretical approach to investigate which environmental factors best explained the variation in breeding success over nearly 50 years (1960–2008). We subsequently combined GLM predictions of breeding success with published survival estimates to project the population trajectory since 1991 (year of maximum population size). In this way, we separated the effects of lemming abundance and population density on population development.4. Breeding success was mainly dependent on lemming abundance, the onset of spring at the breeding grounds, and the population size of brent goose. No evidence was found for carry-over effects (i.e. effects of conditions at main spring staging site). Negative density dependence was operating at a population size above c. 200 000 individuals, but the levelling off of the population could be explained by faltering lemming cycles alone.5. Lemmings have long been known to affect population productivity of Arctic-nesting migratory birds and, more recently, possibly population dynamics of resident bird species, but this is the first evidence for effects of lemming abundance on population size of a migratory bird species. Why lemming cycles are faltering in the last two decades is unclear, but this may be associated with changes in winter climate at Taimyr Peninsula (Siberia).

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.

Monitoring Least Weasels after a Winter Peak of Lemmings in Taimyr: Body Condition, Diet and Habitat Use

Least weasels are highly specialized small-rodent predators. Despite the fact that they are hypothesized to play an important role in generating the lemming cycles, a key process for the functioning of the terrestrial tundra ecosystem, very little is known about the biology of these miniature carnivores in the Arctic. At Mys Vostochny in western Taimyr, Russia, least weasels were observed for the first time during a lemming peak in 2005, but not in two subsequent years with low lemming densities. Here we report observations about weasel signs in lemming winter nests, body condition, habitat use, and diet in summer 2008, a year when lemmings had been numerous under the snow but populations crashed before the summer, and least weasels were abundant. Stable isotope analyses revealed that weasel diet was dominated by Siberian lemmings during spring. As expected, given lower resource availability when the lemming population crashed, weight (taking into account body length) was somewhat lower in 2008 than in 2005. Tracking tunnels and trapping showed that in summer least weasels mostly used sheltered habitats such as rocky outcrops and driftwood. Together with surveys of lemming winter nests, tracking tunnels appeared to be a promising method for monitoring least weasels in the Arctic tundra.

Response of an arctic predator guild to collapsing lemming cycles

Alpine and arctic lemming populations appear to be highly sensitive to climate change, and when faced with warmer and shorter winters, their well-known high-amplitude population cycles may collapse. Being keystone species in tundra ecosystems, changed lemming dynamics may convey significant knock-on effects on trophically linked species. Here, we analyse long-term (1988-2010), community-wide monitoring data from two sites in high-arctic Greenland and document how a collapse in collared lemming cyclicity affects the population dynamics of the predator guild. Dramatic changes were observed in two highly specialized lemming predators: snowy owl and stoat. Following the lemming cycle collapse, snowy owl fledgling production declined by 98 per cent, and there was indication of a severe population decline of stoats at one site. The less specialized long-tailed skua and the generalist arctic fox were more loosely coupled to the lemming dynamics. Still, the lemming collapse had noticeable effects on their reproductive performance. Predator responses differed somewhat between sites in all species and could arise from site-specific differences in lemming dynamics, intra-guild interactions or subsidies from other resources. Nevertheless, population extinctions and community restructuring of this arctic endemic predator guild are likely if the lemming dynamics are maintained at the current non-cyclic, low-density state.