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.

Dietary variation in Icelandic arctic fox (Vulpes lagopus) over a period of 30 years assessed through stable isotopes.

Identifying resources driving long-term trends in predators is important to understand ecosystem changes and to manage populations in the context of conservation or control. The arctic fox population in Iceland has increased steadily over a period of 30 years, an increase that has been attributed to an overall increase in food abundance. We hypothesized that increasing populations of geese or seabirds were driving this growth. We analyzed stable isotopes in a long-term series of collagen samples to determine the role of these different resources. The isotopic signatures of arctic foxes differed consistently between coastal and inland habitats. While δ15N displayed a non-linear change over time with a slight increase in the first part of the period followed by a decline in both habitats, δ13C was stable. Stable isotope mixing models suggested that marine resources and rock ptarmigan were the most important dietary sources, with marine resources dominating in coastal habitats and rock ptarmigan being more important inland. Our results suggest that seabirds may have been driving the arctic fox population increase. The rapidly increasing populations of breeding geese seem to have played a minor role in arctic fox population growth, as rock ptarmigan was the most important terrestrial resource despite a considerable decrease in their abundance during recent decades. This study shows that a long-term population trend in a generalist predator may have occurred without a pronounced change in main dietary resources, despite ongoing structural changes in the food web, where one species of herbivorous birds increased and another decreased.

Interference in the tundra predator guild studied using local ecological knowledge.

The decline or recolonization of apex predators such as wolves and lynx, often driven by management decisions, and the expansion of smaller generalist predators such as red foxes, can have important ecosystem impacts. The mesopredator release hypothesis proposes that apex predators control medium-sized predator populations through competition and/or intraguild predation. The decline of apex predators thus leads to an increase in mesopredators, possibly with a negative impact on prey populations. Information about the abundance of mammalian tundra predators, wolf (Canis lupus), wolverine (Gulo gulo), lynx (Lynx lynx), red fox (Vulpes vulpes) and arctic fox (Vulpes lagopus) was collected from local active outdoors people during semi-structured interviews in 14 low arctic or sub-arctic settlements in western Eurasia. The perceived abundance of red fox decreased with higher wolf abundance and in more arctic areas, but the negative effect of wolves decreased in more arctic and therefore less productive ecosystems. The perceived abundance of arctic fox increased towards the arctic and in areas with colder winters. Although there was a negative correlation between the two fox species, red fox was not included in the model for perceived arctic fox abundance, which received most support. Our results support the mesopredator release hypothesis regarding the expansion of red foxes in subarctic areas and indicate that top-down control by apex predators is weaker in less productive and more arctic ecosystems. We showed that local ecological knowledge is a valuable source of information about large-scale processes, which are difficult to study through direct biological investigations.

Determinants of lemming outbreaks.

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

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

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

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.

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.

Rodent population cycle as a determinant of gastrointestinal nematode abundance in a low-arctic population of the red fox.

We analyzed an 11-year time series (2005-2015) of parasite abundance for three intestinal nematode species in the red fox (Vulpes vulpes) as a function of the multi-annual rodent population cycle in low-arctic Norway, while correcting for other potential covariates that could influence prevalence and abundance. Rodents are paratenic and facultative intermediate hosts for the two Ascarididae species Toxascaris leonina and Toxocara canis, respectively and key prey for the red fox. Still the relative importance of indirect transmission through rodents and direct transmission through free-living stages is unclear. Abundance of these Ascarididae species in individual red foxes (N = 612) exhibited strongly cyclic dynamics that closely mirrored the 4-year rodent cycle. Negative binomial models provided evidence for a direct proportional increase in Ascarididae abundance with rodent density suggesting that predator functional response to rodent prey is the key transmission mechanism. In contrast, no cycles and constantly very low abundance were apparent for Uncinaria stenocephala - a third nematode species recorded without paratenic or intermediate stages.

Unique genetic features of canine adenovirus type 1 (CAdV-1) infecting red foxes (Vulpes vulpes) in northern Norway and arctic foxes (Vulpes lagopus) in Svalbard.

Canine adenovirus type 1 (CAdV-1) is the aetiological agent of infectious canine hepatitis (ICH) in domestic dogs (Canis familiaris). In spite of the widespread use of vaccination, CAdV-1 continues to circulate in the dog population. Although a high number of serological screenings have indicated that CAdV-1 is widespread in fox species, little is known about the potential role of foxes as reservoirs of CAdV-1. Furthermore, very little data exist on the molecular features of this virus in foxes. To add to existing knowledge on CAdV-1 circulating in wild carnivores, tissue samples from CAdV-seropositive red foxes (Vulpes vulpes, n = 10) from the northern mainland of Norway and arctic foxes (Vulpes lagopus, n = 10) from the Svalbard archipelago, Norway, were investigated using a molecular approach to detect CAdV-1 DNA and important structural and non-structural genes of the detected viruses were sequenced and analysed. Amplicons characteristic for CAdV-1 were amplified from 14 out of 20 foxes (7 red foxes and 7 arctic foxes) and spleen and lymph node tissues resulted optimal targets for the viral DNA detection. The nucleotide sequences showed unique features that distinguished the viruses detected in this study from the CAdV-1 to date identified in wild carnivores and dogs. Greater attention should be given to genetically different CAdV-1 circulating in wild carnivores that may be transferred to dogs, potentially causing disease and reducing the effectiveness of available vaccines.

Transferability of biotic interactions: Temporal consistency of arctic plant-rodent relationships is poor.

Variability in biotic interaction strength is an integral part of food web functioning. However, the consequences of the spatial and temporal variability of biotic interactions are poorly known, in particular for predicting species abundance and distribution. The amplitude of rodent population cycles (i.e., peak-phase abundances) has been hypothesized to be determined by vegetation properties in tundra ecosystems. We assessed the spatial and temporal predictability of food and shelter plants effects on peak-phase small rodent abundance during two consecutive rodent population peaks. Rodent abundance was related to both food and shelter biomass during the first peak, and spatial transferability was mostly good. Yet, the temporal transferability of our models to the next population peak was poorer. Plant-rodent interactions are thus temporally variable and likely more complex than simple one-directional (bottom-up) relationships or variably overruled by other biotic interactions and abiotic factors. We propose that parametrizing a more complete set of functional links within food webs across abiotic and biotic contexts would improve transferability of biotic interaction models. Such attempts are currently constrained by the lack of data with replicated estimates of key players in food webs. Enhanced collaboration between researchers whose main research interests lay in different parts of the food web could ameliorate this.

Collapsing population cycles.

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