Siw T. Killengreen

Collapsing population cycles

During the past two decades population cycles in voles, grouse and insects have been fading out in Europe. Here, we discuss the cause and implication of these changes. Several lines of evidence now point to climate forcing as the general underlying cause. However, how climate interacts with demography to induce regime shifts in population dynamics is likely to differ among species and ecosystems. Herbivores with high-amplitude population cycles, such as voles, lemmings, snowshoe hares and forest Lepidoptera, form the heart of terrestrial food web dynamics. Thus, collapses of these cycles are also expected to imply collapses of important ecosystem functions, such as the pulsed flows of resources and disturbances.

Determinants of lemming outbreaks

Population outbreaks in tundra rodents have intrigued scientists for a century as a result of their spectacular appearances and their general lessons in ecology. One outstanding question that has led to competing hypotheses is why sympatric lemmings and voles differ in regularity and shape of their outbreaks. Lemming outbreaks may be lost for decades while vole populations maintain regular population cycles. Moreover, when lemming populations eventually irrupt, they do so more steeply than the vole populations. Norwegian lemmings exhibited a large-scale outbreak synchronously with gray-sided voles in Finnmark, northern Fennoscandia, during 2006 to 2007 for the first time in two decades. Analyses of spatial variability of this outbreak across altitudinal gradients allowed us to identify determinants of the contrasting lemming and vole dynamics. The steeper lemming outbreak trajectories were caused by breeding and population growth during winter, when nonbreeding vole populations consistently declined. The differently shaped lemming and vole outbreaks appear to result from a particular demographic tactic of lemmings that evolved as an adaptation to the long and cold Arctic–Alpine winters. The lemming outbreak amplitude increased with altitude and vole density, indicating that lemming outbreaks are jointly facilitated by low temperatures and apparent mutualism with voles mediated by shared predators. High sensitivity to variation in climate and predation is likely to be the reasons why lemmings have more erratic population dynamics than sympatric voles. The combination of continued climatic warming and dampened vole cycles is expected to further decrease the frequency, amplitude, and geographic range of lemming outbreaks in tundra ecosystems.

The importance of marine vs. human-induced subsidies in the maintenance of an expanding mesocarnivore in the arctic tundra

1. Most studies addressing the causes of the recent increases and expansions of mesopredators in many ecosystems have focused on the top-down, releasing effect of extinctions of large apex predators. However, in the case of the northward expansion of the red fox into the arctic tundra, a bottom-up effect of increased resource availability has been proposed, an effect that can counteract prey shortage in the low phase of the multi-annual rodent cycle. Resource subsidies both with marine and with terrestrial origins could potentially be involved. 2. During different phases of a multi-annual rodent cycle, we investigated the seasonal dynamics and spatial pattern of resource use by red foxes across a coast to inland low arctic tundra gradient, Varanger Peninsula, Norway. We employed two complementary methods of diet analyses: stomach contents and stable isotope analysis. 3. We found that inland red foxes primarily subsisted on reindeer carrions during the low phase of a small rodent population cycle. Lemmings became the most important food item towards the peak phase of the rodent cycle, despite being less abundant than sympatric voles. Isotopic signatures of tissue from both predator and prey also revealed that red foxes near the coast used marine-derived subsidies in the winter, but these allochthonous resources did not spillover to adult foxes living beyond 20-25 km from the coast. 4. Although more needs to be learned about the link between increasing primary productivity due to climatic warming and trophic dynamics in tundra ecosystems, we suggest that changes in reindeer management through a bottom-up effect, at least regionally, may have paved the way towards the establishment of a new mesopredator in the tundra biome.

Carnivore conservation in practice: replicated management actions on a large spatial scale

Summary 1. More than a quarter of the world’s carnivores are threatened, often due to multiple and complex causes. Considerable research efforts are devoted to resolving the mechanisms behind these threats in order to provide a basis for relevant conservation actions. However, even when the underlying mechanisms are known, specific actions aimed at direct support for carnivores are difficult to implement and evaluate at efficient spatial and temporal scales. 2. We report on a 30-year inventory of the critically endangered Fennoscandian arctic fox Vulpes lagopus L., including yearly surveys of 600 fox dens covering 21 000 km 2 . These surveys showed that the population was close to extinction in 2000, with 40–60 adult animals left. However, the population subsequently showed a fourfold increase in size. 3. During this time period, conservation actions through supplementary feeding and predator removal were implemented in several regions across Scandinavia, encompassing 79% of the area. To evaluate these actions, we examined the effect of supplemental winter feeding and red fox control applied at different intensities in 10 regions. A path analysis indicated that 47% of the explained variation in population productivity could be attributed to lemming abundance, whereas winter feeding had a 29% effect and red fox control a 20% effect. 4. This confirms that arctic foxes are highly dependent on lemming population fluctuations but also shows that red foxes severely impact the viability of arctic foxes. This study also highlights the importance of implementing conservation actions on extensive spatial and temporal scales, with geographically dispersed actions to scientifically evaluate the effects. We note that population recovery was only seen in regions with a high intensity of management actions. 5. Synthesis and applications. The present study demonstrates that carnivore population declines may be reversed through extensive actions that target specific threats. Fennoscandian arctic fox is still endangered, due to low population connectivity and expected climate impacts on the distribution and dynamics of lemmings and red foxes. Climate warming is expected to contribute to both more irregular lemming dynamics and red fox appearance in tundra areas; however, the effects of climate change can be mitigated through intensive management actions such as supplemental feeding and red fox control.

Population dynamics of tundra voles in relation to configuration of willow thickets in southern arctic tundra

The areal extent and configuration of thickets of willow shrubs are currently changing in the Arctic both as an effect of global warming and changed browsing pressure of reindeer. These changes have been predicted to impact the distribution and abundance of wildlife species relying on willow thickets as habitat. We assessed the relation between variables quantifying willow thicket configuration and population dynamics of tundra voles (Microtus oeconomus) in three riparian regions in Finnmark, northern Norway, which were subject to intense browsing by semi-domesticated reindeer. The tundra vole, which exhibits 5-year population cycles in Finnmark, is the dominant small rodent species in riparian landscape elements in southern arctic tundra. In the course of a 4-year trapping study, tundra vole populations went through the cyclic phases of increase, peak and crash, however, with distinct differences between the three regions in the population dynamics. Within regions, the occupancy pattern during the increase phase was positively related to willow thicket configuration (in particular edge density and willow height) only in the region attaining the highest abundance and occupancy. However, local abundance was not clearly related to habitat features within any regions. The lack of consistency in the response of tundra vole populations to willow thicket configuration, as well as the positive relation between the degree of thicket shredding and tundra vole habitat occupancy in one of the regions, indicates that tundra voles will not be much affected by climate or browsing induced changes in the shrubbiness of the tundra in the future.

Shedding new light on the diet of Norwegian lemmings: DNA metabarcoding of stomach content

Lemmings are key herbivores in many arctic food webs, and their population dynamics have major impacts on the functioning of tundra systems. However, current knowledge of lemming diet is limited, hampering evaluation of lemming–vegetation interactions. This lack of knowledge is mainly due to methodological challenges, as previously used microhistological methods result in large proportions of poorly resolved plant taxa. We analyzed diets of Norwegian lemmings (Lemmus lemmus) in three different habitats using a new method, DNA metabarcoding of stomach contents. To achieve detailed information on ingested vascular plants, bryophytes, and fungi, we amplified short fragments of chloroplast DNA (for plants; P6 loop of the trnL intron) and nuclear ribosomal DNA (for fungi; ITS1-region). Our results revealed that lemming diets were dominated by grasses, mainly Avenella flexuosa, and mosses, mainly Dicranum spp., but that a variety of other food items were also eaten. Vascular plant composition of the diets differed between heath, meadow, and wetland habitats, whereas bryophyte composition did not. Also, a variety of fungal taxa were retrieved, but as most of the identified taxa belong to micromycetes, they were unlikely to be consumed as food. The role of fungi in the diet of lemmings remains to be investigated. We suggest that there may be substantial variation between habitats and regions in lemming diet.

Indirect food web interactions mediated by predator-rodent dynamics: relative roles of lemmings and voles

Production cycles in birds are proposed as prime cases of indirect interactions in food webs. They are thought to be driven by predators switching from rodents to bird nests in the crash phase of rodent population cycles. Although rodent cycles are geographically widespread and found in different rodent taxa, bird production cycles appear to be most profound in the high Arctic where lemmings dominate. We hypothesized that this may be due to arctic lemmings inducing stronger predator responses than boreal voles. We tested this hypothesis by estimating predation rates in dummy bird nests during a rodent cycle in low-Arctic tundra. Here, the rodent community consists of a spatially variable mix of one lemming (Lemmus lemmus) and two vole species (Myodes rufocanus and Microtus oeconomus) with similar abundances. In consistence with our hypothesis, lemming peak abundances predicted well crash-phase nest predation rates, whereas the vole abundances had no predictive ability. Corvids were found to be the most important nest predators. Lemmings appear to be accessible to the whole predator community which makes them particularly powerful drivers of food web dynamics.

Harmonizing circumpolar monitoring of Arctic fox: benefits, opportunities, challenges and recommendations

ABSTRACT The biodiversity working group of the Arctic Council has developed pan-Arctic biodiversity monitoring plans to improve our ability to detect, understand and report on long-term change in Arctic biodiversity. The Arctic fox (Vulpes lagopus) was identified as a target of future monitoring because of its circumpolar distribution, ecological importance and reliance on Arctic ecosystems. We provide the first exhaustive survey of contemporary Arctic fox monitoring programmes, describing 34 projects located in eight countries. Monitored populations covered equally the four climate zones of the species’ distribution, and there were large differences between populations in long-term trends, multi-annual fluctuations, diet composition, degree of competition with red fox and human interferences. Den density, number of active dens, number of breeding dens and litter size were assessed in almost all populations, while projects varied greatly with respect to monitoring of other variables indicative of population status, ecosystem state or ecosystem function. We review the benefits, opportunities and challenges to increased integration of monitoring projects. We argue that better harmonizing protocols of data collection and data management would allow new questions to be addressed while adding tremendous value to individual projects. However, despite many opportunities, challenges remain. We offer six recommendations that represent decisive progress toward a better integration of Arctic fox monitoring projects. Further, our work serves as a template that can be used to integrate monitoring efforts of other species, thereby providing a key step for future assessments of global biodiversity.

Homage to Hersteinsson and Macdonald: climate warming and resource subsidies cause red fox range expansion and Arctic fox decline

ABSTRACT Climate change can have a marked effect on the distribution and abundance of some species, as well as their interspecific interactions. In 1992, before ecological effects of anthropogenic climate change had developed into a topical research field, Hersteinsson and Macdonald published a seminal paper hypothesizing that the northern distribution limit of the red fox (Vulpes vulpes) is determined by food availability and ultimately climate, while the southern distribution limit of the Arctic fox (Vulpes lagopus) is determined by interspecific competition with the larger red fox. This hypothesis has inspired extensive research in several parts of the circumpolar distribution range of the Arctic fox. Over the past 25 years, it was shown that red foxes can exclude Arctic foxes from dens, space and food resources, and that red foxes kill and sometimes consume Arctic foxes. When the red fox increases to ecologically effective densities, it can cause Arctic fox decline, extirpation and range contraction, while conservation actions involving red fox culling can lead to Arctic fox recovery. Red fox advance in productive tundra, concurrent with Arctic fox retreat from this habitat, support the original hypothesis that climate warming will alter the geographical ranges of the species. However, recent studies show that anthropogenic subsidies also drive red fox advance, allowing red fox establishment north of its climate-imposed distribution limit. We conclude that synergies between anthropogenic subsidies and climate warming will speed up Arctic ecosystem change, allowing mobile species to establish and thrive in human-provided refugia, with potential spill-over effects in surrounding ecosystems.

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

ABSTRACT The 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 territories in summer and from marine and terrestrial carrion in winter. Red fox culling on Varanger Peninsula may have prevented the extirpation of the Arctic fox population. However, one decade after the onset of this management action the Arctic fox population has failed to increase either because the action has been insufficient or because demographic and environmental stochasticity has precluded a positive response. We discuss options for future research and management of the Arctic fox in the Fennoscandian Low Arctic.