Seasonal pulses of migratory prey and annual variation in small mammal abundance affect abundance and reproduction by arctic foxes

We examined how large seasonal influxes of migratory prey influenced population dynamics of arctic foxes and how this varied with fluctuations in small mammal (lemming and vole) abundance—the main prey of arctic foxes throughout most of their range. Specifically, we compared how arctic fox abundance, breeding density and litter size varied inside and outside a large goose colony and in relation to annual variation in small mammal abundance. Information-theoretic model selection showed that (1) breeding density and fox abundance were 2–3 times higher inside the colony than they were outside the colony and (2) litter size, breeding density and annual variation in fox abundance in the colony tracked fluctuations in lemming abundance. The influence of lemming abundance on reproduction and abundance of arctic foxes outside the colony was inconclusive, largely because fox densities outside the colony were low, which made it difficult to detect such relationships. Lemming abundance was, thus, the main factor governing reproduction and abundance of arctic foxes in the colony, whereas seasonal influxes of geese and their eggs provided foxes with external subsidies that elevated breeding density and fox abundance above that which lemmings could support. This study highlights (1) the relative importance of migratory prey and other foods on the abundance and reproduction by local consumers and (2) how migratory animals function as vectors of nutrient transfer between distant ecosystems such as Arctic environments and wintering areas by geese thousands of kilometres to the south.     

The breeding productivity of dark-bellied brent geese and curlew sandpipers in relation to changes in the numbers of arctic foxes and lemmings on the Taimyr Peninsula, Siberia —

There were about three-year cycles in the populations of arctic foxes, and the breeding productivities of brent geese and curlew sandpipers on the Taimyr Peninsula, Russia, The populations of arctic foxes and lemmings changed in synchrony. The breeding productivities of the birds tended to be good when the arctic foxes were increasing in numbers and poor when the arctic foxes were decreasing. There was a negative relationship between arctic fox numbers (or occupied lairs) and the breeding productivity of brent geese in the following year. Although there was evidence of wide-spread synchrony In the lemming cycle across the Taimyr Peninsula, some localities showed differences, However, such sites would still have been influenced by the general pattern of fox abundance in the typical tundra zone of the Taimyr Peninsula, where most of the arctic foxes breed and from which extensive movements of foxes occur after a decline in lemming numbers. The results support a prey-switching hypothesis (also known as the alternative prey hypothesis) whereby arctic foxes, and other predators, feed largely on lemmings when these are abundant or increasing, but switch to birds when the lemming population is small or declining. The relationships between arctic foxes, lemmings and brent geese may be further influenced by snowny owls which create fox-exclusion zones around their nests, thus providing safe nesting areas for the geese.     

Prolonging the arctic pulse: long-term exploitation of cached eggs by arctic foxes when lemmings are scarce

1. Many ecosystems are characterized by pulses of dramatically higher than normal levels of foods (pulsed resources) to which animals often respond by caching foods for future use. However, the extent to which animals use cached foods and how this varies in relation to fluctuations in other foods is poorly understood in most animals. 2. Arctic foxes Alopex lagopus (L.) cache thousands of eggs annually at large goose colonies where eggs are often superabundant during the nesting period by geese. We estimated the contribution of cached eggs to arctic fox diets in spring and autumn, when geese were not present in the study area, by comparing stable isotope ratios (delta(13)C and delta(15)N) of fox tissues with those of their foods using a multisource mixing model in Program IsoSource. 3. The contribution of cached eggs to arctic fox diets was inversely related to collared lemming Dicrostonyx groenlandicus (Traill) abundance; the contribution of cached eggs to overall fox diets increased from < 28% in years when collared lemmings were abundant to 30-74% in years when collared lemmings were scarce. 4. Further, arctic foxes used cached eggs well into the following spring (almost 1 year after eggs were acquired) - a pattern that differs from that of carnivores generally storing foods for only a few days before consumption. 5. This study showed that long-term use of eggs that were cached when geese were superabundant at the colony in summer varied with fluctuations in collared lemming abundance (a key component in arctic fox diets throughout most of their range) and suggests that cached eggs functioned as a buffer when collared lemmings were scarce.     

Predator behaviour and predation risk in the heterogeneous Arctic environment

1. Habitat heterogeneity and predator behaviour can strongly affect predator-prey interactions but these factors are rarely considered simultaneously, especially when systems encompass multiple predators and prey. 2. In the Arctic, greater snow geese Anser caerulescens atlanticus L. nest in two structurally different habitats: wetlands that form intricate networks of water channels, and mesic tundra where such obstacles are absent. In this heterogeneous environment, goose eggs are exposed to two types of predators: the arctic fox Vulpes lagopus L. and a diversity of avian predators. We hypothesized that, contrary to birds, the hunting ability of foxes would be impaired by the structurally complex wetland habitat, resulting in a lower predation risk for goose eggs. 3. In addition, lemmings, the main prey of foxes, show strong population cycles. We thus further examined how their fluctuations influenced the interaction between habitat heterogeneity and fox predation on goose eggs. 4. An experimental approach with artificial nests suggested that foxes were faster than avian predators to find unattended goose nests in mesic tundra whereas the reverse was true in wetlands. Foxes spent 3.5 times more time between consecutive attacks on real goose nests in wetlands than in mesic tundra. Their attacks on goose nests were also half as successful in wetlands than in mesic tundra whereas no difference was found for avian predators. 5. Nesting success in wetlands (65%) was higher than in mesic tundra (56%) but the difference between habitats increased during lemming crashes (15%) compared to other phases of the cycle (5%). Nests located at the edge of wetland patches were also less successful than central ones, suggesting a gradient in accessibility of goose nests in wetlands for foxes. 6. Our study shows that the structural complexity of wetlands decreases predation risk from foxes but not avian predators in arctic-nesting birds. Our results also demonstrate that cyclic lemming populations indirectly alter the spatial distribution of productive nests due to a complex interaction between habitat structure, prey-switching and foraging success of foxes.     

Brent goose colonies near snowy owls: Internest distances in relation to abundance of lemmings and arctic foxes

Brent goose colonies around snowy owl nests have been studied near Medusa Bay (73°21′ N, 80°32′ E) and in the lower reaches of the Uboinaya River (73°37′N, 82°10′E), the northwestern Taimyr Peninsula, from 1999 to 2006. All brent nests within 680 m from an owl nest have been regarded as an individual colony. The results show that the area of the colony is always larger than the protected area around the owl nest. In years of low abundance of lemmings, brent geese nest generally closer to the owl nest than in years of high abundance. When arctic foxes are abundant, however, brent geese nest significantly closer to owls than when the foxes are scarce, irrespective of lemming abundance. The mechanism of brent colony formation around owl nests is based on a number of stimuli.     

The marine side of a terrestrial carnivore: intra-population variation in use of allochthonous resources by arctic foxes

Inter-individual variation in diet within generalist animal populations is thought to be a widespread phenomenon but its potential causes are poorly known. Inter-individual variation can be amplified by the availability and use of allochthonous resources, i.e., resources coming from spatially distinct ecosystems. Using a wild population of arctic fox as a study model, we tested hypotheses that could explain variation in both population and individual isotopic niches, used here as proxy for the trophic niche. The arctic fox is an opportunistic forager, dwelling in terrestrial and marine environments characterized by strong spatial (arctic-nesting birds) and temporal (cyclic lemmings) fluctuations in resource abundance. First, we tested the hypothesis that generalist foraging habits, in association with temporal variation in prey accessibility, should induce temporal changes in isotopic niche width and diet. Second, we investigated whether within-population variation in the isotopic niche could be explained by individual characteristics (sex and breeding status) and environmental factors (spatiotemporal variation in prey availability). We addressed these questions using isotopic analysis and Bayesian mixing models in conjunction with linear mixed-effects models. We found that: i) arctic fox populations can simultaneously undergo short-term (i.e., within a few months) reduction in both isotopic niche width and inter-individual variability in isotopic ratios, ii) individual isotopic ratios were higher and more representative of a marine-based diet for non-breeding than breeding foxes early in spring, and iii) lemming population cycles did not appear to directly influence the diet of individual foxes after taking their breeding status into account. However, lemming abundance was correlated to proportion of breeding foxes, and could thus indirectly affect the diet at the population scale.     

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.     

Indirect effects of lemming cycles on sandpiper dynamics: 50 years of counts from southern Sweden

The bird-lemming hypothesis postulates that breeding success of tundra-nesting geese and waders in Siberia follows the cyclic pattern of lemming populations, as a result of predators switching from lemmings to birds when the lemming population crashes. We present 50 years of data on constant-effort catches of red knot Calidris canutus and curlew sandpiper C. ferruginea at an autumn migratory stopover site (Ottenby) at the Baltic Sea, supplemented with literature data on winter censuses of dark-bellied brent goose Branta b. bernicla and white-fronted goose Anser albifrons in northwestern Europe, and waders in Germany and Southern Africa. Number and proportion of juveniles in these bird populations (both our own and literature data) were compared with an index of predation pressure (calculated from the abundance of lemmings on the Taimyr peninsula), and climate indices for the North Eurasia and the North Atlantic regions. The index of predation pressure correlated significantly with the number of juveniles of red knot and curlew sandpiper, but not with number of adults. Also, this index correlated with the reproductive performance of geese and waders reported in the literature. Fourier analysis revealed a significant deviation from random noise with the maximum spectral density at the period length of 3 years for number of juvenile red knots and curlew sandpipers captured at Ottenby, abundance of lemmings, reproduction in arctic fox Alopex lagopus, and reproductive performance in geese on the Siberian tundra. Also, the date of passage at Ottenby for adult red knot and curlew sandpiper showed a spectral density peak at a period length of 3 years, the latter species also showing a peak at a period length of 5-6 years. Passage dates for adult red knot and curlew sandpiper were earlier in years of high predation pressure compared with years of low predation pressure. The fluctuations in reproductive success of the studied Siberian goose and wader species appear to be primarily influenced by biotic factors in the breeding area, rather than by abiotic factors, such as climate oscillations. Annual variations in migratory arctic bird populations may have far reaching effects in habitats along their migration routes and in their wintering areas. We suggest a link between lemming cyclicity in the Northern Hemisphere and predation pressure on Southern Hemisphere benthos, in which the signal is carried between continents by long distance migrating waders.     

Habitat selection,reproduction and predation of wintering lemmings in the Arctic

Snow cover has dramatic effects on the structure and functioning of Arctic ecosystems in winter. In the tundra, the subnivean space is the primary habitat of wintering small mammals and may be critical for their survival and reproduction. We have investigated the effects of snow cover and habitat features on the distributions of collared lemming (Dicrostonyx groenlandicus) and brown lemming (Lemmus trimucronatus) winter nests, as well as on their probabilities of reproduction and predation by stoats (Mustela erminea) and arctic foxes (Vulpes lagopus). We sampled 193 lemming winter nests and measured habitat features at all of these nests and at random sites at two spatial scales. We also monitored overwinter ground temperature at a subsample of nest and random sites. Our results demonstrate that nests were primarily located in areas with high micro-topography heterogeneity, steep slopes, deep snow cover providing thermal protection (reduced daily temperature fluctuations) and a high abundance of mosses. The probability of reproduction increased in collared lemming nests at low elevation and in brown lemming nests with high availability of some graminoid species. The probability of predation by stoats was density dependent and was higher in nests used by collared lemmings. Snow cover did not affect the probability of predation of lemming nests by stoats, but deep snow cover limited predation attempts by arctic foxes. We conclude that snow cover plays a key role in the spatial structure of wintering lemming populations and potentially in their population dynamics in the Arctic.     

Are goose nesting success and lemming cycles linked? Interplay between nest density and predators

The suggested link between lemming cycles and reproductive success of arctic birds is caused by potential effects of varying predation pressure (the Alternative Prey Hypothesis, APH) and protective association with birds of prey (the Nesting Association Hypothesis, NAH). We used data collected over two complete lemming cycles to investigate how fluctuations in lemming density were associated with nesting success of greater snow geese ( Anser caerulescens atlanticus ) in the Canadian High Arctic. We tested predictions of the APH and NAH for geese breeding at low and high densities. Goose nesting success varied from 22% to 91% between years and the main egg predator was the arctic fox ( Alopex lagopus ). Nesting associations with snowy owls ( Nyctea scandiaca ) were observed but only during peak lemming years for geese nesting at low density. Goose nesting success declined as distance from owls increased and reached a plateau at 550 m. Artificial nest experiments indicated that owls can exclude predators from the vicinity of their nests and thus reduce goose egg predation rate. Annual nest failure rate was negatively associated with rodent abundance and was generally highest in low lemming years. This relationship was present even after excluding goose nests under the protective influence of owls. However, nest failure was inversely density-dependent at high breeding density. Thus, annual variations in nest density influenced the synchrony between lemming cycles and oscillations in nesting success. Our results suggest that APH is the main mechanism linking lemming cycles and goose nesting success and that nesting associations during peak lemming years (NAH) can enhance this positive link at the local level. The study also shows that breeding strategies used by birds (the alternative prey) could affect the synchrony between oscillations in avian reproductive success and rodent cycles.     

Brent goose colonies near snowy owls: Internest distances in relation to breeding arctic fox densities

It was shown that in the years when the numbers of the Arctic foxes are high, even though the lemming numbers are high as well, Brent geese nest considerably closer to owls’ nests than in the years with low Arctic fox numbers. At values of the Arctic fox densities greater than one breeding pair per 20 km², the factor of lemming numbers ceases to affect the distance between owl and geese nests. This distance becomes dependent on the Arctic fox density (numbers). When the Arctic fox density is greater than the pronounced threshold, the owl-Brent internest distance is inversely and linearly related to the Arctic fox density.     

Trophic interactions in a high arctic snow goose colony

We examined the role of trophic interactions in structuringa high arctic tundra community characterized by a large breedingcolony of greater snow geese (Chen caerulescens atlantica).According to the exploitation ecosystem hypothesis of Oksanenet al. (1981), food chains are controlled by top-down interactions.However, because the arctic primary productivity is low, herbivorepopulations are too small to support functional predator populationsand these communities should thus be dominated by the plant/herbivore trophic-level interaction. Since 1990, we have beenmonitoring annual abundance and productivity of geese, the impactof goose grazing, predator abundance (mostly arctic foxes, Alopexlagopus) and the abundance of lemmings, the other significantherbivore in this community, on Bylot Island, Nunavut, Canada.Goose grazing consistently removed a significant proportionof the standing crop (     

Predator‐mediated interactions between preferred,alternative and incidental prey in the arctic tundra

Apparent competition between prey is hypothesized to occur more frequently in environments with low densities of preferred prey, where predators are forced to forage for multiple prey items. In the arctic tundra, numerical and functional responses of predators to preferred prey (lemmings) affect the predation pressure on alternative prey (goose eggs) and predators aggregate in areas of high alternative prey density. Therefore, we hypothesized that predation risk on incidental prey (shorebird eggs) would increase in patches of high goose nest density when lemmings were scarce. To test this hypothesis, we measured predation risk on artificial shorebird nests in quadrats varying in goose nest density on Bylot Island (Nunavut, Canada) across three summers with variable lemming abundance. Predation risk on artificial shorebird nests was positively related to goose nest density, and this relationship was strongest at low lemming abundance when predation risk increased by 600% as goose nest density increased from 0 to 12 nests ha^?1. Camera monitoring showed that activity of arctic foxes, the most important predator, increased with goose nest density. Our data support our incidental prey hypothesis; when preferred prey decrease in abundance, predator mediated apparent competition via aggregative response occurs between the alternative and incidental prey items.     

Diet of arctic foxes (Alopex lagopus) in Iceland

Arctic foxes, Alopex lagopus , live in low productivity arctic and northern tundra habitats, where they generally prey heavily on lemmings. In Iceland, however, no lemmings are present, and the foxes have a very varied diet, including plants such as seaweed and black crowberries, a wide range of birds and invertebrates, and carcasses of large mammals such as seals, reindeer, and sheep. Marked seasonal, geographical and inter-annual differences confirm arctic foxes in Iceland as opportunistic feeders. There are coastal and inland foxes: coastal foxes feed mainly on prey derived directly or indirectly from the ocean, particularly various seabirds and seals, while inland foxes feed largely on migrant birds, such as geese, waders and passerines in summer, and ptarmigan in winter. Despite their reputation for killing lambs, in this study, lamb carcasses were found at only 19.4% of 1125 fox dens, 44% of which had only one carcass. The distance to the nearest farm and the physical condition of lambs were major determinants of the number of carcasses found at a den. We discuss the implications of arctic foxes' diet for population dynamics and group formation, and for management practices.     

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.     

Common ravens raid arctic fox food caches

Cache recovery is critical for evolution of hoarding behaviour, because the energy invested in caching may be lost if consumers other than the hoarders benefit from the cached food. By raiding food caches, animals may exploit the caching habits of others, that should respond by actively defending their caches. The arctic fox (Alopex lagopus) is the main predator of lemmings and goose eggs in the Canadian High Arctic and stores much of its prey in the ground. Common ravens (Corvus corax) are not as successful as foxes in taking eggs from goose nests. This generalist avian predator regularly uses innovation and opportunism to survive in many environments. Here, we provide the first report that ravens can successfully raid food cached by foxes, and that foxes may defend their caches from ravens.     

Brent Geese (<Emphasis Type="Italic">Branta bernicla</Emphasis>) Breeding Associations with Pomarine Skuas (<Emphasis Type="Italic">Stercorarius pomarinus</Emphasis>) on the Mainland Tundra

This article is based on data that were collected in the years 2000?2007, 2012, and 2014 in the vicinities of Medusa Bay (73°21′ N, 80°32′ E) and in 2002 at the mouth of the Uboynaya River (73°37′ N, 82°10′ E), in the northwestern part of the Taimyr Peninsula. In years when the abundance of lemmings is high, brent geese may breed not only near nests of snowy owls and rough-legged buzzards, but also sparsely in the mainland tundra, often without any protection. Some such nests are successfully incubated until hatching. A considerable part of these dispersed nests appears to be associated with a nest or territory of pomarine skuas that are able to scare away the main tundra predator, the arctic fox, to a distance of about 500 m from their nests. Brent geese that breed within this distance to theses nests gain additional protection against arctic foxes. However, brent geese do not display a tendency to place their nests closer to pomarine skua nests. The mean distance from geese nests to pomarine skua nests or centers of their territories comprised 2/3 of the mean distance between nests of pomarine skuas and turned out to be quite stable over the years and in two different tundra areas.     

Red-breasted goose colonies on the Taimyr Peninsula: Factors responsible for the proximity of goose nests to nests of peregrine falcons,rough-legged buzzards,and snowy owls

Red-breasted goose colonies have been studied near Medusa Bay (73°21′N, 80°32′E), on the northwestern Taimyr Peninsula, and along the Agapa River (70°11′N, 86°15′E) down to its mouth (71°26′N, 89° 13′E), in the central Taimyr Peninsula. Red-breasted geese nesting near peregrine falcons are protected by the falcons from arctic foxes; however, they are sometimes attacked by the falcons themselves. In the colonies near peregrine falcon nests, the vast majority of goose nests were situated no farther than 100 m from the falcon nest. When food is abundant, falcons protect a larger area around their nest. The distance between the falcon nest and the surrounding goose nests is inversely related to the falcon’s activity. In years of higher falcon activity, falcons prevent red-breasted geese from nesting as close to their nest as in years of lower falcon activity. Additional stimuli are required for red-breasted geese to form colonies near rough-legged buzzard nests. The distance between snowy owl nests and red-breasted goose nests was smaller when arctic foxes were abundant than when they were scarce.     

Farmed arctic foxes on the Fennoscandian mountain tundra: implications for conservation

Hybridization between wild and captive-bred individuals is a serious conservation issue that requires measures to prevent negative effects. Such measures are, however, often considered controversial by the public, especially when concerning charismatic species. One of the threats to the critically endangered Fennoscandian arctic fox Alopex lagopus is hybridization with escaped farm foxes, conveying a risk of outbreeding depression through loss of local adaptations to the lemming cycle. In this study, we investigate the existence of escaped farm foxes among wild arctic foxes and whether hybridization has occurred in the wild. We analysed mitochondrial control region sequences and 10 microsatellite loci in samples from free-ranging foxes and compared them with reference samples of known farm foxes and true Fennoscandian arctic foxes. We identified the farm fox specific mitochondrial haplotype H9 in 25 out of 182 samples, 21 of which had been collected within or nearby the wild subpopulation on Hardangervidda in south-western Norway. Genetic analyses of museum specimens collected on Hardangervidda (1897–1975) suggested that farm fox genotypes have recently been introduced to the area. Principal component analysis as well as both model- and frequency-based analyses of microsatellite data imply that the free-ranging H9s were farm foxes rather than wild arctic foxes and that the entire Hardangervidda population consisted of farm foxes or putative hybrids. We strongly recommend removal of farm foxes and hybrids in the wild to prevent genetic pollution of the remaining wild subpopulations of threatened arctic foxes.     

Predation of arctic fox (<Emphasis Type="Italic">Vulpes lagopus</Emphasis>) pups by common ravens (<Emphasis Type="Italic">Corvus corax</Emphasis>)

Identifying correctly trophic interactions is important for understanding population dynamics and ecosystem functioning. However, some predator–prey relationships may still remain undetected, due to the difficulty of observing rare predation events. We report the first observation of predation of arctic fox (Vulpes lagopus) pups by common ravens (Corvus corax). The predation event was witnessed on Bylot Island, Nunavut, Canada, through an automatic camera placed on a den. On June 8, 2013, the day following pup emergence from the den, the complete litter of four was killed and taken away by a pair of ravens despite the intermittent presence of the mother. This event lasted 2.5 h, occurred during a low lemming year, and resulted in the fox pair failing their reproduction. Only two other fox litters were present that summer in our 600 km² study area, so this litter predated by ravens accounted for 25 % (4/16) of the pups produced. Our report shows how continuous monitoring of dens using automatic cameras can allow documentation of rare events. In addition to food competition and cache raiding, pup predation contributes to the antagonistic interactions between arctic foxes and ravens in the High Arctic, which may intensify during low lemming years. This observation allows a better understanding of species interactions within the Arctic predator guild.