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.

Predator co-occurrence in alpine and Arctic tundra in relation to fluctuating prey.

Large carnivores influence ecosystem dynamics in multiple ways, for example, by suppressing meso-carnivores and providing carrions for smaller scavengers. Loss of large carnivores is suggested to cause meso-carnivore increase and expansion. Moreover, competition between meso-carnivores may be modified by the presence of larger carnivores. In tundra ecosystems, the smallest meso-carnivore, the Arctic fox, has experienced regional declines, whereas its larger and competitively superior congener, the red fox, has increased, potentially due to changes in the abundance of apex predators. We explored if variation in the occurrence of wolverine and golden eagle impacted the occurrence and co-occurrence of the Arctic fox and red fox in relation to varying abundances of small rodents within the Scandinavian tundra. We applied multi-species occupancy models to an extensive wildlife camera dataset from 2011-2020 covering 98 sites. Daily detection/non-detection of each species per camera trap site and study period (late winter; March-May) was stacked across years, and species occupancy was related to small rodent abundance while accounting for time of the year and status of simulated carcass. The Arctic fox was more likely to co-occur with the red fox when the wolverine was present and less likely to co-occur with the red fox when golden eagles were present and the wolverine was absent. Red foxes increased in occupancy when co-occurring with the larger predators. The Arctic fox responded more strongly to small rodent abundance than the red fox and co-occurred more often with the other species at carcasses when rodent abundance was low. Our findings suggest that the interspecific interactions within this tundra predator guild appear to be surprisingly intricate, driven by facets of fear of predation, interspecific mediation and facilitation, and food resource dynamics. These dynamics of intraguild interactions may dictate where and when conservation actions targeted towards the Arctic fox should be implemented.

Estimating red fox density using non-invasive genetic sampling and spatial capture-recapture modelling.

Spatial capture-recapture modelling (SCR) is a powerful tool for estimating density, population size, and space use of elusive animals. Here, we applied SCR modelling to non-invasive genetic sampling (NGS) data to estimate red fox (Vulpes vulpes) densities in two areas of boreal forest in central (2016-2018) and southern Norway (2017-2018). Estimated densities were overall lower in the central study area (mean = 0.04 foxes per km2 in 2016, 0.10 in 2017, and 0.06 in 2018) compared to the southern study area (0.16 in 2017 and 0.09 in 2018). We found a positive effect of forest cover on density in the central, but not the southern study area. The absence of an effect in the southern area may reflect a paucity of evidence caused by low variation in forest cover. Estimated mean home-range size in the central study area was 45 km2 [95%CI 34-60] for females and 88 km2 [69-113] for males. Mean home-range sizes were smaller in the southern study area (26 km2 [16-42] for females and 56 km2 [35-91] for males). In both study areas, detection probability was session-dependent and affected by sampling effort. This study highlights how SCR modelling in combination with NGS can be used to efficiently monitor red fox populations, and simultaneously incorporate ecological factors and estimate their effects on population density and space use.

Fur colour in the Arctic fox: genetic architecture and consequences for fitness.

Genome-wide association studies provide good opportunities for studying the genetic basis of adaptive traits in wild populations. Yet, previous studies often failed to identify major effect genes. In this study, we used high-density single nucleotide polymorphism and individual fitness data from a wild non-model species. Using a whole-genome approach, we identified the MC1R gene as the sole causal gene underlying Arctic fox Vulpes lagopus fur colour. Further, we showed the adaptive importance of fur colour genotypes through measures of fitness that link ecological and evolutionary processes. We found a tendency for blue foxes that are heterozygous at the fur colour locus to have higher fitness than homozygous white foxes. The effect of genotype on fitness was independent of winter duration but varied with prey availability, with the strongest effect in years of increasing rodent populations. MC1R is located in a genomic region with high gene density, and we discuss the potential for indirect selection through linkage and pleiotropy. Our study shows that whole-genome analyses can be successfully applied to wild species and identify major effect genes underlying adaptive traits. Furthermore, we show how this approach can be used to identify knowledge gaps in our understanding of interactions between ecology and evolution.

Fitness and fur colouration: Testing the camouflage and thermoregulation hypotheses in an Arctic mammal.

Selection for crypsis has been recognized as an important ecological driver of animal colouration, whereas the relative importance of thermoregulation is more contentious with mixed empirical support. A potential thermal advantage of darker individuals has been observed in a wide range of animal species. Arctic animals that exhibit colour polymorphisms and undergo seasonal colour moults are interesting study subjects for testing the two alternative hypotheses: demographic performance of different colour morphs might be differentially affected by snow cover with a cryptic advantage for lighter morphs, or conversely by winter temperature with a thermal advantage for darker morphs. In this study, we explored whether camouflage and thermoregulation might explain differences in reproduction and survival between the white and blue colour morphs of the Arctic fox Vulpes lagopus under natural conditions. Juvenile and adult survival, breeding propensity and litter size were measured for 798 captive-bred and released or wild-born Arctic foxes monitored during an 11-year period (2007-2017) in two subpopulations in south-central Norway. We investigated the proportion of the two colour morphs and compared their demographic performance in relation to spatial variation in duration of snow cover, onset of snow season and winter temperatures. After population re-establishment, a higher proportion of blue individuals was observed among wild-born Arctic foxes compared to the proportion of blue foxes released from the captive population. Our field study provides the first evidence for an effect of colour morph on the reproductive performance of Arctic foxes under natural conditions, with a higher breeding propensity of the blue morph compared to the white one. Performance of the two colour morphs was not differentially affected by the climatic variables, except for juvenile survival. Blue morph juveniles showed a tendency for higher survival under colder winter temperatures but lower survival under warmer temperatures compared to white morph juveniles. Overall, our findings do not consistently support predictions of the camouflage or the thermoregulation hypotheses. The higher success of blue foxes suggests an advantage of the dark morph not directly related to disruptive selection by crypsis or thermoregulation. Our results rather point to physiological adaptations and behavioural traits not necessarily connected to thermoregulation, such as stress response, immune function, sexual behaviour and aggressiveness. Our findings highlight the need to explore the potential role of genetic linkage or pleiotropy in influencing the fitness of white and blue Arctic foxes as well as other species with colour polymorphisms.

Genetic rescue in an inbred Arctic fox (Vulpes lagopus) population.

Isolation of small populations can reduce fitness through inbreeding depression and impede population growth. Outcrossing with only a few unrelated individuals can increase demographic and genetic viability substantially, but few studies have documented such genetic rescue in natural mammal populations. We investigate the effects of immigration in a subpopulation of the endangered Scandinavian arctic fox (Vulpes lagopus), founded by six individuals and isolated for 9 years at an extremely small population size. Based on a long-term pedigree (105 litters, 543 individuals) combined with individual fitness traits, we found evidence for genetic rescue. Natural immigration and gene flow of three outbred males in 2010 resulted in a reduction in population average inbreeding coefficient (f), from 0.14 to 0.08 within 5 years. Genetic rescue was further supported by 1.9 times higher juvenile survival and 1.3 times higher breeding success in immigrant first-generation offspring compared with inbred offspring. Five years after immigration, the population had more than doubled in size and allelic richness increased by 41%. This is one of few studies that has documented genetic rescue in a natural mammal population suffering from inbreeding depression and contributes to a growing body of data demonstrating the vital connection between genetics and individual fitness.

Genetic footprints reveal geographic patterns of expansion in Fennoscandian red foxes.

Population expansions of boreal species are among the most substantial ecological consequences of climate change, potentially transforming both structure and processes of northern ecosystems. Despite their importance, little is known about expansion dynamics of boreal species. Red foxes (Vulpes vulpes) are forecasted to become a keystone species in northern Europe, a process stemming from population expansions that began in the 19th century. To identify the relative roles of geographic and demographic factors and the sources of northern European red fox population expansion, we genotyped 21 microsatellite loci in modern and historical (1835-1941) Fennoscandian red foxes. Using Bayesian clustering and Bayesian inference of migration rates, we identified high connectivity and asymmetric migration rates across the region, consistent with source-sink dynamics, whereby more recently colonized sampling regions received immigrants from multiple sources. There were no clear clines in allele frequency or genetic diversity as would be expected from a unidirectional range expansion from south to north. Instead, migration inferences, demographic models and comparison to historical red fox genotypes suggested that the population expansion of the red fox is a consequence of dispersal from multiple sources, as well as in situ demographic growth. Together, these findings provide a rare glimpse into the anatomy of a boreal range expansion and enable informed predictions about future changes in boreal communities.

Subclinical thiamine deficiency results in failed reproduction in Arctic foxes.

Thiamine deficiency can result in life-threatening physiological and neurological complications. While a thiamine-deficient diet may result in the onset of such symptoms, the presence of thiaminase - an enzyme that breaks down thiamine - is very often the cause. In such instances, thiaminase counteracts the bioavailability and uptake of thiamine, even when food-thiamine levels are adequate. Here, we report on a case of failed reproduction in seven Arctic fox (Vulpes lagopus) breeding pairs kept at a captive breeding facility, including the presentation of severe thiamine deficiency symptoms in two male foxes. Symptoms included ataxia, obtundation, truncal sway, star-gazing and visual impairment. Blood tests were inconclusive, yet symptoms resolved following treatment with a series of thiamine hydrochloride injections, thereby verifying the diagnosis. A fish-dominated feed, which for the first time had been frozen for a prolonged period, was identified as the likely source of thiaminase and subsequent deterioration in the animals' health. Symptoms in the two males arose during the annual mating period. All seven breeding pairs at the captive breeding station failed to reproduce - a phenomenon never recorded during the captive breeding facility's preceding 17-year operation. Relating our findings to peer-reviewed literature, the second part of this case report assesses how thiamine deficiency (due to thiaminase activity) likely resulted in subclinical effects that impaired the production of reproduction hormones, and thereby led to a complete breeding failure. While previous work has highlighted the potentially lethal effects of thiamine deficiency in farmed foxes, this is, to our knowledge the first study showing how subclinical effects in both males and females may inhibit reproduction in foxes in general, but specifically Arctic foxes. The findings from our case report are not only relevant for captive breeding facilities, but for the welfare and management of captive carnivorous animals in general.

Life history traits in a cyclic ecosystem: a field experiment on the arctic fox.

The reproduction of many species depends strongly on variation in food availability. The main prey of the arctic fox in Fennoscandia are cyclic small rodents, and its number of litters and litter size vary depending on the phase of the rodent cycle. In this experiment, we studied if the arctic fox adjusts its reproduction as a direct response to food abundance, in accordance with the food limitation hypothesis, or if there are additional phase-dependent trade-offs that influence its reproduction. We analysed the weaning success, i.e. proportion of arctic fox pairs established during mating that wean a litter in summer, of 422 pairs of which 361 were supplementary winter fed, as well as the weaned litter size of 203 litters of which 115 were supplementary winter fed. Females without supplementary winter food over-produced cubs in relation to food abundance in the small rodent increase phase, i.e. the litter size was equal to that in the peak phase when food was more abundant. The litter size for unfed females was 6.38 in the increase phase, 7.11 in the peak phase and 3.84 in the decrease phase. The litter size for supplementary winter-fed litters was 7.95 in the increase phase, 10.61 in the peak phase and 7.86 in the decrease phase. Thus, feeding had a positive effect on litter size, but it did not diminish the strong impact of the small rodent phase, supporting phase-dependent trade-offs in addition to food determining arctic fox reproduction.

Predation of endangered Arctic foxes by Golden eagles: What do we know?

Dedicated conservation efforts spanning the past two decades have saved the Fennoscandian Arctic fox (Vulpes lagopus) population from local extinction, and extensive resources continue to be invested in the species' conservation and management. Although increasing, populations remain isolated, small and are not yet viable in the longer term. An understanding of causes of mortality are consequently important to optimize ongoing conservation actions. Golden eagles (Aquila chrysaetos) are a predator of Arctic foxes, yet little information on this interaction is available in the literature. We document and detail six confirmed cases of Golden eagle depredation of Arctic foxes at the Norwegian captive breeding facility (2019-2022), where foxes are housed in large open-air enclosures in the species' natural habitat. Here, timely detection of missing/dead foxes was challenging, and new insights have been gained following recently improved enclosure monitoring. Golden eagle predation peaked during the winter months, with no cases reported from June to November. This finding contrasts with that which is reported from the field, both for Arctic and other fox species, where eagle depredation peaked at dens with young (summer). While the seasonality of depredation may be ecosystem specific, documented cases from the field may be biased by higher survey efforts associated with the monitoring of reproductive success during the summer. Both white and blue color morphs were housed at the breeding station, yet only white foxes were preyed upon, and mortality was male biased. Mitigation measures and their effectiveness implemented at the facility are presented. Findings are discussed in the broader Arctic fox population ecology and conservation context.

Reproductive responses to spatial and temporal prey availability in a coastal Arctic fox population.

1. Input of external subsidies in the Arctic may have substantial effects on predator populations that otherwise would have been limited by low local primary productivity. 2. We explore life-history traits, age-specific fecundity, litter sizes and survival, and the population dynamics of an Arctic fox (Vulpes lagopus) population to explore the influence of the spatial distribution and temporal availability of its main prey; including both resident and migrating (external) prey resources. 3. This study reveals that highly predictable cross-boundary subsidies from the marine food web, acting through seasonal access to seabirds, sustain larger local Arctic fox populations. Arctic fox dens located close to the coast in Svalbard were found to have higher occupancy rates, as expected from both high availability and high temporal and spatial predictability of prey resources (temporally stable external subsidies). Whereas the occupancy rate of inland dens varied between years in relation to the abundance of reindeer carcasses (temporally varying resident prey). 4. With regard to demography, juvenile Arctic foxes in Svalbard have lower survival rates and a high age of first reproduction compared with other populations. We suggest this may be caused by a lack of unoccupied dens and a saturated population.

Climate influence on plant-pollinator interactions in the keystone species Vaccinium myrtillus.

Climate change is altering the world's ecosystems through direct effects of climate warming and precipitation changes but also indirectly through changes in biotic interactions. For instance, climate-driven changes in plant and/or insect communities may alter plant-pollinator interactions, thereby influencing plant reproductive success and ultimately population dynamics of insect-pollinated plants. To better understand how the importance of insect pollination for plant fruit set varies with climate, we experimentally excluded pollinators from the partly selfing keystone species Vaccinium myrtillus along elevational gradients in the forest-tundra ecotone in central Norway. The study comprised three mountain areas, seven elevational gradients spanning from the climatically relatively benign birch forest to the colder alpine areas above the tree line, and 180 plots of 1 × 1 m, with experimental treatments allocated randomly to plots within sites. Within the experimental plots, we counted the number of flowers of V. myrtillus and counted and weighed all fruits, as well as seeds for a selection of fruits. Excluding pollinators resulted in lower fruit production, as well as reduced fruit and seed mass of V. myrtillus. In the alpine sites pollinator exclusion resulted in 84% fewer fruits, 50% lower fruit weight, and 50% lower seed weight compared to control conditions. Contrary to our expectations, the negative effect of pollinator exclusion was less pronounced in the forest compared to alpine sites, suggesting that the importance of insect pollination for seed production is lower at low elevations. Our findings indicate that the keystone species V. myrtillus is relatively robust to changes in the pollinator community in a warmer climate, thereby making it less vulnerable to climate-driven changes in plant-pollinator interactions.

Genomic Consequences of Fragmentation in the Endangered Fennoscandian Arctic Fox (Vulpes lagopus).

Accelerating climate change is causing severe habitat fragmentation in the Arctic, threatening the persistence of many cold-adapted species. The Scandinavian arctic fox (Vulpes lagopus) is highly fragmented, with a once continuous, circumpolar distribution, it struggled to recover from a demographic bottleneck in the late 19th century. The future persistence of the entire Scandinavian population is highly dependent on the northernmost Fennoscandian subpopulations (Scandinavia and the Kola Peninsula), to provide a link to the viable Siberian population. By analyzing 43 arctic fox genomes, we quantified genomic variation and inbreeding in these populations. Signatures of genome erosion increased from Siberia to northern Sweden indicating a stepping-stone model of connectivity. In northern Fennoscandia, runs of homozygosity (ROH) were on average ~1.47-fold longer than ROH found in Siberia, stretching almost entire scaffolds. Moreover, consistent with recent inbreeding, northern Fennoscandia harbored more homozygous deleterious mutations, whereas Siberia had more in heterozygous state. This study underlines the value of documenting genome erosion following population fragmentation to identify areas requiring conservation priority. With the increasing fragmentation and isolation of Arctic habitats due to global warming, understanding the genomic and demographic consequences is vital for maintaining evolutionary potential and preventing local extinctions.

Pulses of movement across the sea ice: population connectivity and temporal genetic structure in the arctic fox.

Lemmings are involved in several important functions in the Arctic ecosystem. The Arctic fox (Vulpes lagopus) can be divided into two discrete ecotypes: "lemming foxes" and "coastal foxes". Crashes in lemming abundance can result in pulses of "lemming fox" movement across the Arctic sea ice and immigration into coastal habitats in search for food. These pulses can influence the genetic structure of the receiving population. We have tested the impact of immigration on the genetic structure of the "coastal fox" population in Svalbard by recording microsatellite variation in seven loci for 162 Arctic foxes sampled during the summer and winter over a 5-year period. Genetic heterogeneity and temporal genetic shifts, as inferred by STRUCTURE simulations and deviations from Hardy-Weinberg proportions, respectively, were recorded. Maximum likelihood estimates of movement as well as STRUCTURE simulations suggested that both immigration and genetic mixture are higher in Svalbard than in the neighbouring "lemming fox" populations. The STRUCTURE simulations and AMOVA revealed there are differences in genetic composition of the population between summer and winter seasons, indicating that immigrants are not present in the reproductive portion of the Svalbard population. Based on these results, we conclude that Arctic fox population structure varies with time and is influenced by immigration from neighbouring populations. The lemming cycle is likely an important factor shaping Arctic fox movement across sea ice and the subsequent population genetic structure, but is also likely to influence local adaptation to the coastal habitat and the prevalence of diseases.

Scavenger community structure along an environmental gradient from boreal forest to alpine tundra in Scandinavia.

Scavengers can have strong impacts on food webs, and awareness of their role in ecosystems has increased during the last decades. In our study, we used baited camera traps to quantify the structure of the winter scavenger community in central Scandinavia across a forest-alpine continuum and assess how climatic conditions affected spatial patterns of species occurrences at baits. Canonical correspondence analysis revealed that the main habitat type (forest or alpine tundra) and snow depth was main determinants of the community structure. According to a joint species distribution model within the HMSC framework, species richness tended to be higher in forest than in alpine tundra habitat, but was only weakly associated with temperature and snow depth. However, we observed stronger and more diverse impacts of these covariates on individual species. Occurrence at baits by habitat generalists (red fox, golden eagle, and common raven) typically increased at low temperatures and high snow depth, probably due to increased energetic demands and lower abundance of natural prey in harsh winter conditions. On the contrary, occurrence at baits by forest specialists (e.g., Eurasian jay) tended to decrease in deep snow, which is possibly a consequence of reduced bait detectability and accessibility. In general, the influence of environmental covariates on species richness and occurrence at baits was lower in alpine tundra than in forests, and habitat generalists dominated the scavenger communities in both forest and alpine tundra. Following forecasted climate change, altered environmental conditions are likely to cause range expansion of boreal species and range contraction of typical alpine species such as the arctic fox. Our results suggest that altered snow conditions will possibly be a main driver of changes in species community structure.

Documenting lemming population change in the Arctic: Can we detect trends?

Lemmings are a key component of tundra food webs and changes in their dynamics can affect the whole ecosystem. We present a comprehensive overview of lemming monitoring and research activities, and assess recent trends in lemming abundance across the circumpolar Arctic. Since 2000, lemmings have been monitored at 49 sites of which 38 are still active. The sites were not evenly distributed with notably Russia and high Arctic Canada underrepresented. Abundance was monitored at all sites, but methods and levels of precision varied greatly. Other important attributes such as health, genetic diversity and potential drivers of population change, were often not monitored. There was no evidence that lemming populations were decreasing in general, although a negative trend was detected for low arctic populations sympatric with voles. To keep the pace of arctic change, we recommend maintaining long-term programmes while harmonizing methods, improving spatial coverage and integrating an ecosystem perspective.

Correction to: Documenting lemming population change in the Arctic: Can we detect trends?

In the original published article, some of the symbols in figure 1A were modified incorrectly during the typesetting and publication process. The correct version of the figure is provided in this correction.

Consequences of past climate change and recent human persecution on mitogenomic diversity in the arctic fox.

Ancient DNA provides a powerful means to investigate the timing, rate and extent of population declines caused by extrinsic factors, such as past climate change and human activities. One species probably affected by both these factors is the arctic fox, which had a large distribution during the last glaciation that subsequently contracted at the start of the Holocene. More recently, the arctic fox population in Scandinavia went through a demographic bottleneck owing to human persecution. To investigate the consequences of these processes, we generated mitogenome sequences from a temporal dataset comprising Pleistocene, historical and modern arctic fox samples. We found no evidence that Pleistocene populations in mid-latitude Europe or Russia contributed to the present-day gene pool of the Scandinavian population, suggesting that postglacial climate warming led to local population extinctions. Furthermore, during the twentieth-century bottleneck in Scandinavia, at least half of the mitogenome haplotypes were lost, consistent with a 20-fold reduction in female effective population size. In conclusion, these results suggest that the arctic fox in mainland Western Europe has lost genetic diversity as a result of both past climate change and human persecution. Consequently, it might be particularly vulnerable to the future challenges posed by climate change. This article is part of a discussion meeting issue 'The past is a foreign country: how much can the fossil record actually inform conservation?'

Serosurvey for canine distemper virus, canine adenovirus, Leptospira interrogans, and Toxoplasma gondii in free-ranging canids in Scandinavia and Svalbard.

Prevalence of antibodies reactive to canine distemper virus (CDV), canine adenovirus type 1 (CAV-1), Leptospira interrogans serovars Canicola and Icterohaemorrhagiae, and Toxoplasma gondii were examined in free-ranging Scandinavian canids. Sampling included 275 red foxes (Vulpes vulpes) from mainland Norway, 60 arctic foxes (Vulpes lagopus) from the high-arctic islands of Svalbard, and 98 wolves (Canis lupus) from the joint Swedish-Norwegian population. Methods used included virus neutralization tests for CDV and CAV-1, a microscopic agglutination test for L. interrogans, and a direct agglutination test for T. gondii. High prevalence of antibody to CAV-1 was identified in red foxes (59.6%), wolves (67.7%), and arctic foxes (37.8%). The prevalence of antibody to CDV varied between 9.6% and 12.3% in the three species. Antibodies to L. interrogans serovar Icterohaemorrhagiae were found in 9.9% of the red foxes and 8.4% of the wolves sampled, whereas no antibody-positive arctic foxes were found. All animals were antibody-negative for L. interrogans serovar Canicola. Antibodies to T. gondii were found in 66.9, 51.7, and 18.6% of red foxes, arctic foxes and wolves, respectively. Significantly more adults than juveniles were antibody-positive for CDV in red foxes and arctic foxes, for CAV-1 in wolves, and for T. gondii in red foxes and wolves. There was a general tendency for adult female red foxes to have a higher prevalence of antibodies for CDV than adult males; this difference was statistically significant. The results indicate that CDV and CAV-1 are endemic in red foxes and wolves on the Scandinavian mainland and in arctic foxes on Svalbard. Although infection with L. interrogans serovar Icterohaemorrhagiae was relatively common in wild canids on mainland Norway, it was not found on Svalbard, where the maintenance host (Rattus norvegicus) is absent. All three species are commonly exposed to T. gondii through predation on infected intermediate hosts.

Spatial distribution of Echinococcus multilocularis, Svalbard, Norway.

In Svalbard, Norway, the only intermediate host for Echinococcus multilocularis, the sibling vole, has restricted spatial distribution. A survey of feces from the main host, the arctic fox, showed that only the area occupied by the intermediate host is associated with increased risk for human infection.