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.     

Exclusion by interference competition? The relationship between red and arctic foxes

The distribution of many predators may be limited by interactions with larger predator species. The arctic fox in mainland Europe is endangered, while the red fox is increasing its range in the north. It has been suggested that the southern distribution limit of the arctic fox is determined by interspecific competition with the red fox. This has been criticised, on the basis that the species co-exist on a regional scale. However, if the larger red fox is superior and interspecific competition important, the arctic fox should avoid close contact, especially during the breeding season. Consequently, the distribution of breeding dens for the two species would be segregated on a much smaller spatial and temporal scale, in areas where they are sympatric. We tested this hypothesis by analysing den use of reproducing arctic and red foxes over 9 years in Sweden. High quality dens were inhabited by reproducing arctic foxes more often when no red foxes bred in the vicinity. Furthermore, in two out of three cases when arctic foxes did reproduce near red foxes, juveniles were killed by red foxes. We also found that breeding arctic foxes occupied dens at higher altitudes than red foxes did. In a large-scale field experiment, red foxes were removed, but the results were not conclusive. However, we conclude that on the scale of individual territories, arctic foxes avoid areas with red foxes. Through interspecific interference competition, the red fox might thus be excluding the arctic fox from breeding in low altitude habitat, which is most important in years when food abundance is limited and competition is most fierce. With high altitude refuges being less suitable, even small-scale behavioural effects could scale up to significant effects at the population level.     

From breeding pairs to fox towns: the social organisation of arctic fox populations with stable and fluctuating availability of food

Food availability can impact group formation in Carnivora. Specifically, it has been suggested that temporal variation in food availability may allow a breeding pair to tolerate additional adults in their territory at times when food abundance is high. We investigate group occurrence and intraspecific tolerance during breeding in a socially flexible canid, the arctic fox (Vulpes lagopus). We compare Iceland and Sweden where resource conditions differ considerably. A breeding pair was the most common social unit in both populations, but as predicted, groups were more frequent where food abundance varied substantially between years (Sweden: 6 %) than where food availability was stable (Iceland: ≤2 %). Within Sweden, supplemental feeding increased group occurrence from 6 to 21 %, but there was no effect of natural variation in lemming (Lemmus lemmus) availability since group formation was rare also at lemming highs. Thus, additional factors appeared to influence the trade-off between intraspecific territoriality and tolerance. We report two cases where related females showed enduring social relationships with good-neighbour strategies. Related females also engaged in alloparental behaviour in a ‘fox town’ with 31 foxes (4 adults, 3 litters). In contrast, when unrelated foxes bred close to each other, they moved or split their litters during summer, presumably because of territorial conflict. We suggest that fluctuating food availability is linked to group formation in this Arctic carnivore, but also when food availability increases, additional factors such as relatedness, alloparental benefits, competition and predator defence appear necessary to explain group formation.     

Natal den selection by sympatric arctic and red foxes on Herschel Island,Yukon, Canada

In the twentieth century, red fox (Vulpes vulpes) expanded into the Canadian Arctic, where it competes with arctic fox (Vulpes lagopus) for food and shelter. Red fox dominates in physical interactions with the smaller arctic fox, but little is known about competition between them on the tundra. On Hershel Island, north Yukon, where these foxes are sympatric, we focused on natal den choice, a critical aspect of habitat selection. We tested the hypothesis that red fox displaces arctic fox from dens in prey-rich habitats. We applied an approach based on model comparisons to analyse a 10-year data set and identify factors important to den selection. Red fox selected dens in habitats that were more prey-rich in spring. When red foxes reproduced, arctic fox selected dens with good springtime access, notably many burrows unblocked by ice and snow. These provided the best refuge early in the reproductive season. In the absence of red foxes, arctic foxes selected dens offering good shelter (i.e. large isolated dens). Proximity to prey-rich habitats was consistently less important than the physical aspects of dens for arctic fox. Our study shows for the first time that red foxes in the tundra select dens associated primarily with prey-rich areas, while sympatric arctic foxes do not. These results fit a model of red fox competitively interfering with arctic fox, the first detailed study of such competition in a true arctic setting.     

Food limitation and social regulation in a red fox population

This study evaluates a conceptual model on functional and numerical response to short-term fluctuating vole populations of a red fox ( Vulpes vulpes L.) population in south-central Sweden. The model assumes that this particular population is located in between socially regulated stable populations to the south and direct food-limited populations to the north. The model predicts: (1) food availability as the primary factor for limiting fox numbers, causing reduced rates of reproduction and survival during years of low vole densities, and (2) density-dependent regulation during years of increasing and high vole densities resulting in increased group sizes within territories of fixed dimensions. During 1973–1980 data were obtained from 1216 fox scats, 874 fox carcasses, 63 tagged foxes, nine radio-collared females and from yearly den counts in an area of 130 km², Eight predictions of the model were tested. These concerned the occurrence of small rodents in fox diet, fluctuations in the density of foxes, variations in the number of fox litters, the effect on reproduction of providing supplemental food during January–May, the proportion of vixens bearing a litter different years, dispersal of young males relative to that of young females throughout the vole cycle, and variations in mortality rates of young males and females. All tests were in favour of the conceptual model, and contradictory to alternative models.     

Inter- and intraspecific competition between the fox species Alopex lagopus and Vulpes vulpes: an evaluation trial under penned conditions

This study compared competition capacity and dominance relations between arctic foxes (Alopex lagopus) and red foxes (Vulpes vulpes). Experiments were carried out in semi-natural earthen floor enclosures using farm-bred colour types of both species (blue fox and silver fox) as subjects. Results of the dominance scoring and open field behaviour after weaning in August-September showed that blue foxes dominated over silver foxes. Thereafter, the situation gradually became reversed and silver foxes were dominant during the breeding and whelping seasons. Housing both species together from weaning produced more curious animals as compared to when these species were placed in common quarters after the autumn equinox. In the case of blue foxes, the male dominated highly over all females. In silver foxes, the difference in dominance between the sexes was, however, less pronounced. The most dominant individuals in the study groups were typically among the heaviest. Breedings and whelpings succeeded better in silver than in blue foxes. However, none of litters born survived more than one week. The present results support the conclusion that when both fox species are housed together, Vulpus vulpus tends to dominate over Alopex lagopus. Received: 22 March 1996/Accepted: 30 June 1996     

Use of Supplementary Feeding Dispensers by Arctic Foxes in Norway

Supplementary feeding is often used as a conservation tool to reverse the decline of food-limited populations. The arctic fox (Vulpes lagopus) is one of the most endangered mammals in Norway and has been the target of several conservation initiatives for almost 3 decades, including supplementary feeding. To measure and improve the efficiency of supplementary feeding as a conservation action, we used passive integrated transponder (PIT)-tags in arctic foxes and 6 feeding stations equipped with PIT-tag readers to monitor individual use of supplemental food between 2013 and 2018. We tested hypotheses about the potential influence of temporal and spatial patterns, individual characteristics (i.e., age, sex, reproductive status), and food abundance (abundance of small rodents and amount of food filled) on the frequency and intensity of use of supplementary feeding stations by arctic foxes. The feeding stations were visited ≥1 time by 196 PIT-tagged individuals. We detected 54% of juveniles born in the study area between 2013 and 2017 at the feeding stations. More arctic foxes used the feeding stations during the pre-breeding period than during the other seasons, and the visits occurred mostly at night. The closest feeding station to each natal den was systematically used by the established pair and by the juveniles born at this den. Juveniles did not use the feeding stations more than adult foxes. Older foxes, and breeding adults, visited the feeding stations more than younger and non-breeding adults. Foxes used feeding stations more intensively when prey was scarce and with greater amounts of supplemental food. This study highlights that supplemental feeding is important for breeding adults, especially in periods of low prey abundance. Understanding the use of feeding stations will contribute to the optimization of supplemental feeding as a conservation action and help wildlife managers to carefully plan and manage its discontinuation. © 2020 The Authors. Journal of Wildlife Management published by Wiley Periodicals, Inc. on behalf of The Wildlife Society.     

Distinct patterns in alpine vegetation around dens of the Arctic fox

The arctic fox Alopex lagopus excavates its dens in gravely ridges and hillocks, and creates a local environment quite distinct from the surrounding tundra or heath landscape. In northern Sweden, the vegetation of 18 dens of the arctic fox was investigated, as well as reference areas off the dens but in geologically and topographically similar locations. The species composition showed considerable differences between den and reference areas, with grasses and forbs occurring more abundantly on the dens, and evergreen dwarf-shrubs occurring more in reference areas. The effect of the foxes' activities is thought to be either through mechanical soil disturbance, or through nutrient enrichment via scats, urine, and carcasses. This was expected to result in differences in plant traits with key functional roles in resource acquisition and regeneration, when comparing dens with reference areas. We hypothesised that the community mean of specific leaf area (SLA) would differ if nutrient enrichment was the more important effect, and that seed weight, inversely proportional to seed number per ramet and hence dispersal ability, would differ if soil disturbance was the more important effect. Specific leaf area showed a significant difference, indicating nutrient enrichment to be the most important effect of the arctic fox on the vegetation on its dens. Arctic foxes act as ecosystems engineers on a small scale, maintaining niches for relatively short-lived nutrient demanding species on their dens in spite of the dominance of long-lived ericaceous dwarf-shrubs in the landscape matrix. Thus, foxes contribute to the maintenance of species richness on the landscape level.     

Dominance relations in captive groups of adult and juvenile arctic blue foxes (Alopex lagopus)

Dominance relationships were studied in captive Arctic blue fox (Alopex lagopus) groups comprising adults (four males, five females) and juveniles (four males, five females). The results showed that Arctic blue foxes easily formed a social organization with an observable hierarchy, in which adults typically dominated over juveniles. Within the same age group, males usually dominated over females. Dominance correlated most significantly with body weight in autumn, but later that correlation decreased. Urine marking activity was very low during autumn and early winter, but increased significantly prior to and during the breeding season when aggressive encounters were also most pronounced. In addition to several adults, the social status of some juveniles was high at breeding time. Altogether 7 out of 11 females (63.6%) whelped, but the survival rate of litters was low and kits of only two adult females survived (18.2%). It can be concluded that hierarchical development and reproduction in Arctic blue fox groups are markedly influenced by dominance relationships.     

Arctic fox versus red fox in the warming Arctic: four decades of den surveys in north Yukon

During the last century, the red fox (Vulpes vulpes) has expanded its distribution into the Arctic, where it competes with the arctic fox (Vulpes lagopus), an ecologically similar tundra predator. The red fox expansion correlates with climate warming, and the ultimate determinant of the outcome of the competition between the two species is hypothesized to be climate. We conducted aerial and ground fox den surveys in the northern Yukon (Herschel Island and the coastal mainland) to investigate the relative abundance of red and arctic foxes over the last four decades. This region has undergone the most intense warming observed in North America, and we hypothesized that this climate change led to increasing dominance of red fox over arctic fox. Results of recent surveys fall within the range of previous ones, indicating little change in the relative abundance of the two species. North Yukon fox dens are mostly occupied by arctic fox, with active red fox dens occurring sympatrically. While vegetation changes have been reported, there is no indication that secondary productivity and food abundance for foxes have increased. Our study shows that in the western Arctic of North America, where climate warming was intense, the competitive balance between red and arctic foxes changed little in 40?years. Our results challenge the hypotheses linking climate to red fox expansion, and we discuss how climate warming’s negative effects on predators may be overriding positive effects of milder temperatures and longer growing seasons.     

Inheritance of litter size at birth in farmed arctic foxes (Alopex lagopus, Canidae, Carnivora)

Natural populations of the arctic fox (Alopex lagopus, Canidae, Carnivora) differ drastically in their reproductive strategy. Coastal foxes, which depend on stable food resources, produce litters of moderate size. Inland foxes feed on small rodents, whose populations are characterized by cycling fluctuation. In the years with low food supply, inland fox populations have a very low rate of reproduction. In the years with high food supply, they undergo a population explosion. To gain insight into the genetic basis of the reproductive strategy of this species, we performed complex segregation analysis of the litter size in the extended pedigree of the farmed arctic foxes involving 20,665 interrelated animals. Complex segregation analysis was performed using a mixed model assuming that the trait was under control of a major gene and a large number of additive genetic and random factors. To check the significance of any major gene effect, we used Elston-Stewart transmission probability test. Our analysis demonstrated that the inheritance of this trait can be described within the frameworks of a major gene model with recessive control of low litter size. This model was also supported by the pattern of its familial segregation and by comparison of the distributions observed in the population and that expected under our model. We suggest that a system of balanced polymorphism for litter size in the farmed population might have been established in natural populations of arctic foxes as a result of adaptation to the drastic fluctuations in prey availability.     

The food habits of arctic fox (<Emphasis Type="Italic">Alopex lagopus semenovi</Emphasis>) reproductive families on mednyi island (Commander Islands)

In total, 1406 samples of scat of 19 arctic fox families and 1755 prey remains collected near the dens of 32 families during the cub rearing period were analyzed. This is the first attempt to evaluate the food use in the population according to averaged data for a large number of families. After the population had passed through the bottleneck, the arctic fox diet changed considerably. Colonies of petrels—the northern fulmar Fulmarus glacialis rodgersii and the storm-petrels Oceanodroma furcata and O. leucorhoa—became the main food source, whereas the use of alternative resources (alcids, cormorants, marine invertebrates, and otarid rookery products) decreased considerably. The following factors are assumed to determine the arctic fox foraging strategy, i.e., the selectivity in food acquisition: (1) passing of the population through the bottleneck; (2) termination of anthropogenic influence due to the liquidation of human settlements on the island; (3) decrease in both the bird populations and abundance of marine invertebrates (sea urchins and mussels); and (4) stable low density of the current arctic fox population. A hypothetical scenario for formation of the foraging specialization in the island population is discussed.     

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.     

Arctic Fox Responses to Tourism Activity

As the interest for nature-based tourism activities increases, it is important to provide evidence-based guidelines for wildlife-human interactions to minimize the disturbance caused to wildlife. In Fennoscandia, the endangered arctic fox (Vulpes lagopus) is subject to increasing tourism interest and some regions recommend a minimum approach distance of 300 m, but the guidelines have not been scientifically validated. We conducted experimental human approaches towards arctic fox den sites to study activity and behavioral changes in response to the approaching observer. The first arctic foxes hid when approached within 300 m, but many had increased their vigilance already at the start distance of 500 m. At approximately 200 m, the hiding probability increased rapidly at dens disturbed and undisturbed by tourism activities. Arctic foxes at disturbed dens allowed the observer to approach more closely before they increased their vigilance and before they hid compared to foxes at undisturbed dens. We confirm that a minimum distance of 300 m might be sufficient for most arctic foxes to refrain from hiding, but a longer distance would be required to avoid causing any disturbance. We recommend a minimum approach distance of ≥300 m to be implemented in all Fennoscandian regions inhabited by the arctic fox. © 2020 The Wildlife Society.     

Finding the right home: distribution of food resources and terrain characteristics influence selection of denning sites and reproductive dens in arctic foxes

We examined 83 arctic fox (Alopex lagopus) dens on Bylot Island (Canada) during the summers of 2003–2005, to determine how arctic foxes select a denning site among potential sites, and a breeding den among existing dens. We compared denning sites to random locations in a 425 km² study area (landscape scale) and to other potential denning sites in a 100 m radius (local scale). Dens were located on mounds or in slopes and were closer to streams than expected. Sites with low snow cover in spring, high ground temperature, high depth to permafrost, and steep and southerly exposed slopes were preferred. Of the 83 dens, 27 were used at least once for reproduction from 2003 to 2005. We show with a resource selection function analysis that an attractive force (distribution of food resources) and an apparently repulsive one (presence of other dens in the vicinity) affected selection of dens for reproduction. We generate testable hypotheses regarding the influence of food and social factors on the denning ecology of arctic foxes. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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.     

Predator–prey relationships: arctic foxes and lemmings

1. The number of breeding dens and litter sizes of arctic foxes Alopex lagopus were recorded and the diet of the foxes was analysed during a ship-based expedition to 17 sites along the Siberian north coast. At the same time the cyclic dynamics of co-existing lemming species were examined.
2. The diet of arctic foxes was dominated by the Siberian lemming Lemmus sibiricus (on one site the Norwegian lemming L. lemmus ), followed by the collared lemming Dicrostonyx torquatus .
3. The examined Lemmus sibiricus populations were in different phases of the lemming cycle as determined by age profiles and population densities.
4. The numerical response of arctic foxes to varying densities of Lemmus had a time lag of 1 year, producing a pattern of limit cycles in lemming–arctic fox interactions. Arctic fox litter sizes showed no time lag, but a linear relation to Lemmus densities. We found no evidence for a numerical response to population density changes in Dicrostonyx .
5. The functional or dietary response of arctic foxes followed a type II curve for Lemmus , but a type III response curve for Dicrostonyx .
6. Arctic foxes act as resident specialist for Lemmus and may increase the amplitude and period of their population cycles. For Dicrostonyx , on the other hand, arctic foxes act as generalists which suggests a capacity to dampen oscillations.     

The fluctuating world of a tundra predator guild: bottom‐up constraints overrule top‐down species interactions in winter

Global warming is predicted to change ecosystem functioning and structure in Arctic ecosystems by strengthening top‐down species interactions, i.e. predation pressure on small herbivores and interference between predators. Yet, previous research is biased towards the summer season. Due to greater abiotic constraints, Arctic ecosystem characteristics might be more pronounced in winter. Here we test the hypothesis that top‐down species interactions prevail over bottom‐up effects in Scandinavian mountain tundra (Northern Sweden) where effects of climate warming have been observed and top‐down interactions are expected to strengthen. But we test this ‘a priori’ hypothesis in winter and throughout the 3–4 yr rodent cycle, which imposes additional pulsed resource constraints. We used snowtracking data recorded in 12 winters (2004–2015) to analyse the spatial patterns of a tundra predator guild (arctic fox Vulpes lagopus, red fox Vulpes vulpes, wolverine Gulo gulo) and small prey (ptarmigan, Lagopus spp). The a priori top‐down hypothesis was then tested through structural equation modelling, for each phase of the rodent cycle. There was weak support for this hypothesis, with top‐down effects only discerned on arctic fox (weakly, by wolverine) and ptarmigan (by arctic fox) at intermediate and high rodent availability respectively. Overall, bottom‐up constraints appeared more influential on the winter community structure. Cold specialist predators (arctic fox and wolverine) showed variable landscape associations, while the boreal predator (red fox) appeared strongly dependent on productive habitats and ptarmigan abundance. Thus, we suggest that the unpredictability of food resources determines the winter ecology of the cold specialist predators, while the boreal predator relies on resource‐rich habitats. The constraints imposed by winters and temporary resource lows should therefore counteract productivity‐driven ecosystem change and have a stabilising effect on community structure. Hence, the interplay between summer and winter conditions should determine the rate of Arctic ecosystem change in the context of global warming.     

Temporal variability in arctic fox diet as reflected in stable-carbon isotopes; the importance of sea ice

Consumption of marine foods by terrestrial predators can lead to increased predator densities, potentially impacting their terrestrial resources. For arctic foxes (Alopex lagopus), access to such marine foods in winter depends on sea ice, which is threatened by global climate change. To quantify the importance of marine foods (seal carrion and seal pups) and document temporal variation in arctic fox diet I measured the ratios of the stable isotopes of carbon (¹³C/¹²C) in hair of arctic foxes near Cape Churchill, Manitoba, from 1994 to 1997. These hair samples were compared to the stable carbon isotope ratios of several prey species. Isotopic differences between seasonally dimorphic pelage types indicated a diet with a greater marine content in winter when sea ice provided access to seal carrion. Annual variation in arctic fox diet in both summer and winter was correlated with lemming abundance. Marine food sources became much more important in winters with low lemming populations, accounting for nearly half of the winter protein intake following a lemming decline. Potential alternative summer foods with isotopic signatures differing from lemmings included goose eggs and caribou, but these were unavailable in winter. Reliance on marine food sources in winter during periods of low lemming density demonstrates the importance of the sea ice as a potential habitat for this arctic fox population and suggests that a continued decline in sea ice extent will disrupt an important link between the marine and terrestrial ecosystems.     

Prevalence and geographical distribution of the ear canker mite (Otodectes cynotis) among arctic foxes (Alopex lagopus) in Iceland

Three hundred forty five adult arctic foxes (Alopex lagopus) from all counties in Iceland were examined for excess cerumen and ear canker mites (Otodectes cynotis). Only 13 foxes (4%) from a single county in northwestern Iceland were infested, where the prevalence of otodectiasis was 38%. Whether or not this parasite is new to the arctic fox in Iceland is unknown. If it is recently introduced, possible sources of infestation are farmed silver foxes (Vulpes vulpes), domestic dogs, domestic or feral cats, and arctic foxes from Greenland. It appears that the rate of transmission between adult foxes is low; a more common route of transmission is probably from the mother to her offspring or between vixens breeding in the same dens in subsequent years by contamination of the dens. No correlation was found between the prevalence of mites in foxes and Samson character.