Lemming winter habitat: the quest for warm and soft snow.

During the cold arctic winter, small mammals like lemmings seek refuge inside the snowpack to keep warm and they dig tunnels in the basal snow layer, usually formed of a soft depth hoar, to find vegetation on which they feed. The snowpack, however, is a heterogenous medium and lemmings should use habitats where snow properties favor their survival and winter reproduction. We determined the impact of snow physical properties on lemming habitat use and reproduction in winter by sampling their winter nests for 13 years and snow properties for 6 years across 4 different habitats (mesic, riparian, shrubland, and wetland) on Bylot Island in the Canadian High Arctic. We found that lemmings use riparian habitat most intensively because snow accumulates more rapidly, the snowpack is the deepest and temperature of the basal snow layer is the highest in this habitat. However, in the deepest snowpacks, the basal depth hoar layer was denser and less developed than in habitats with shallower snowpacks, and those conditions were negatively related to lemming reproduction in winter. Shrubland appeared a habitat of moderate quality for lemmings as it favored a soft basal snow layer and a deep snowpack compared with mesic and wetland, but snow conditions in this habitat critically depend on weather conditions at the beginning of the winter. With climate change, a hardening of the basal layer of the snowpack and a delay in snow accumulation are expected, which could negatively affect the winter habitat of lemmings and be detrimental to their populations.

Combining deep sequencing and conventional molecular approaches reveals broad diversity and distribution of fleas and Bartonella in rodents and shrews from Arctic and Subarctic ecosystems.

BACKGROUND: Bartonella are intracellular bacteria that are transmitted via animal scratches, bites and hematophagous arthropods. Rodents and their associated fleas play a key role in the maintenance of Bartonella worldwide, with > 22 species identified in rodent hosts. No studies have addressed the occurrence and diversity of Bartonella species and vectors for small mammals in Arctic and Subarctic ecosystems, which are increasingly impacted by invasive species and climate change. METHODS: In this study, we characterized the diversity of rodent fleas using conventional PCR targeting the mitochondrial cytochrome c oxidase II gene (COII) and Bartonella species in rodents and shrews (n = 505) from northern Canada using conventional PCR targeting the ITS (intergenic transcribed spacer) region and gltA (citrate synthase) gene. Metagenomic sequencing of a portion of the gltA gene was completed on a subset of 42 rodents and four rodent flea pools. RESULTS: Year, total summer precipitation the year prior to sampling, average minimum spring temperature and small mammal species were significant factors in predicting Bartonella positivity. Occurrence based on the ITS region was more than double that of the gltA gene and was 34% (n = 349) in northern red-backed voles, 35% (n = 20) in meadow voles, 37% (n = 68) in deer mice and 31% (n = 59) in shrews. Six species of Bartonella were identified with the ITS region, including B. grahamii, B. elizabethae, B. washoensis, Candidatus B. rudakovii, B. doshiae, B. vinsonii subsp. berkhoffii and subsp. arupensis. In addition, 47% (n = 49/105) of ITS amplicons had < 97% identity to sequences in GenBank, possibly due to a limited reference library or previously unreported species. An additional Bartonella species (B. heixiaziensis) was detected during metagenomic sequencing of the gltA gene in 6/11 rodents that had ITS sequences with < 97% identity in GenBank, highlighting that a limited reference library for the ITS marker likely accounted for low sequence similarity in our specimens. In addition, one flea pool from a northern red-backed vole contained multiple species (B. grahamii and B. heixiaziensis). CONCLUSION: Our study calls attention to the usefulness of a combined approach to determine the occurrence and diversity of Bartonella communities in hosts and vectors.

Density-dependent demography and movements in a cyclic brown lemming population.

Theoretical modeling predicts that both direct and delayed density-dependence are key factors to generate population cycles. Deciphering density-dependent processes that lead to variable population growth characterizing different phases of the cycles remains challenging. This is particularly the case for the period of prolonged low densities, which is inherently data deficient. However, demographic analyses based on long-term capture-mark-recapture datasets can help resolve this question. We relied on a 16-year (2004-2019) live-trapping program to analyze the summer demography and movements of a cyclic brown lemming population in the Canadian Arctic. More specifically, we examined if inversely density-dependent processes could explain why population growth can remain low during the prolonged low phase. We found that the proportion of females in the population was inversely density-dependent with a strong male-biased sex ratio at low densities but not at high densities. However, survival of adult females was higher than adult males, but both had lower survival at low densities than at high ones. Distances moved by both adult males and females were density-dependent, and proportion of females in reproductive condition was weakly density-dependent as it tended to increase at low density. Individual body condition, measured as monthly change in body mass, was not density-dependent. Overall, the strong male-biased sex ratio at very low densities suggests a loss of reproductive potential due to the rarity of females and appears to be the most susceptible demographic factor that could contribute to the prolonged low phase in cyclic brown lemmings. What leads to this sex-bias in the first place is still unclear, potentially owing to our trapping period limited to the summer, but we suggest that it could be due to high predation rate on breeding females in winter.

Ultra-light photosensor collars to monitor Arctic lemming activity.

Background: Studying the anti-predatory behavior of mammals represents an important challenge, especially for fossorial small mammals that hide in burrows. In the Arctic, such behaviors are critical to the survival of lemmings considering that predation risks are high every summer. Because detailed information about how lemmings use burrows as hideouts is still lacking, we developed a 1.59 g photosensitive collar to record any event of a small mammal moving between a dark area (e.g., burrow) and a bright area (e.g., outside the burrow). Tests of how collars affected lemming behavior were conducted in captivity in Cambridge Bay, Nunavut, Canada, in November 2019 and field tests were conducted on Bylot Island, Nunavut, Canada, in August 2021. Results: The device was made of two chemical batteries and a printed circuit board (PCB) equipped with a photosensor and a real-time clock that recorded amplitude transient thresholds of light (lux) continuously. In accordance with ethical use of such devices, we verified that no abnormal loss of body mass was observed in captive or free-ranging lemmings, and no difference in recapture rates were observed between those with and without a collar, though we could not test this for periods longer than 108 h. Measurements of light intensities revealed consistent patterns with high lux levels at mid-day and lowest during the night. Lemmings showed clearly defined behavioral patterns alternating between periods outside and inside burrows. Despite 24-h daylight in the middle of the summer, August nighttime (i.e., 11 PM to 4 AM) lux levels were insufficient for amplitude transient thresholds to be reached. Conclusion: By taking advantage of the long periods of daylight in the Arctic, such technology is very promising as it sets new bases for passive recording of behavioral parameters and builds on the prospect of further miniaturization of batteries and PCBs.

Climate variability and density-dependent population dynamics: Lessons from a simple High Arctic ecosystem.

Ecologists are still puzzled by the diverse population dynamics of herbivorous small mammals that range from high-amplitude, multiannual cycles to stable dynamics. Theory predicts that this diversity results from combinations of climatic seasonality, weather stochasticity, and density-dependent food web interactions. The almost ubiquitous 3- to 5-y cycles in boreal and arctic climates may theoretically result from bottom-up (plant-herbivore) and top-down (predator-prey) interactions. Assessing, empirically, the roles of such interactions and how they are influenced by environmental stochasticity has been hampered by food web complexity. Here, we take advantage of a uniquely simple High Arctic food web, which allowed us to analyze the dynamics of a graminivorous vole population not subjected to top-down regulation. This population exhibited high-amplitude, noncyclic fluctuations-partly driven by weather stochasticity. However, the predominant driver of the dynamics was overcompensatory density dependence in winter that caused the population to frequently crash. Model simulations showed that the seasonal pattern of density dependence would yield regular 2-y cycles in the absence of stochasticity. While such short cycles have not yet been observed in mammals, they are theoretically plausible if graminivorous vole populations are deterministically bottom-up regulated. When incorporating weather stochasticity in the model simulations, cyclicity became disrupted and the amplitude was increased-akin to the observed dynamics. Our findings contrast with the 3- to 5-y population cycles that are typical of graminivorous small mammals in more complex food webs, suggesting that top-down regulation is normally an important component of such dynamics.

Seasonal food webs with migrations: multi-season models reveal indirect species interactions in the Canadian Arctic tundra.

Models incorporating seasonality are necessary to fully assess the impact of global warming on Arctic communities. Seasonal migrations are a key component of Arctic food webs that still elude current theories predicting a single community equilibrium. We develop a multi-season model of predator-prey dynamics using a hybrid dynamical systems framework applied to a simplified tundra food web (lemming-fox-goose-owl). Hybrid systems models can accommodate multiple equilibria, which is a basic requirement for modelling food webs whose topology changes with season. We demonstrate that our model can generate multi-annual cycling in lemming dynamics, solely from a combined effect of seasonality and state-dependent behaviour. We compare our multi-season model to a static model of the predator-prey community dynamics and study the interactions between species. Interestingly, including seasonality reveals indirect interactions between migrants and residents not captured by the static model. Further, we find that the direction and magnitude of interactions between two species are not necessarily accurate using only summer time-series. Our study demonstrates the need for the development of multi-season models and provides the tools to analyse them. Integrating seasonality in food web modelling is a vital step to improve predictions about the impacts of climate change on ecosystem functioning. This article is part of the theme issue 'The changing Arctic Ocean: consequences for biological communities, biogeochemical processes and ecosystem functioning'.

Resource partitioning among avian predators of the Arctic tundra.

Interspecific competition can play a key role in structuring ecological communities. The Arctic tundra is a low productivity ecosystem supporting simple food webs, but several predators often feed on the same prey species, lemmings, known for their large-amplitude population fluctuations. We examined mechanisms involved in reducing intra-guild competition and allowing coexistence of four avian predators (snowy owls, glaucous gulls, rough-legged hawks and long-tailed jaegers) feeding on a pulsed resource (brown and collared lemmings). We compared the size and species of prey consumed by predators to see if resource partitioning occurred. We also verified if spatial segregation in nesting areas could be another mechanism allowing coexistence. Finally, we tested if the absence of the snowy owl, a dominant and irruptive species, triggered a competitive release on the smallest predator, the jaeger, with respect to prey size and nesting area used. We monitored the breeding of predators and lemming abundance over a 14-year period on Bylot Island, Canada. We mapped their nesting sites and collected regurgitation pellets to recover lemming mandibles, which were used to infer prey species and size. The size of lemmings consumed varied among species with the largest predators consuming the largest lemmings and the smallest predators consuming the smallest lemmings. All predators consumed more collared than brown lemmings compared to their availability although owls and jaegers consumed relatively more brown lemmings compared to gulls and hawks. Jaegers consumed larger lemmings in the absence of owls than in their presence, suggestive of a short-term competitive release. We found moderate to low overlap in nesting areas among predators and no evidence of their expansion in the absence of owls, suggesting that spatial distribution is caused by species-specific habitat preferences. The main mechanism to partition food resources among these avian predators is spatial segregation, and secondarily prey size and species. However, we found evidence that food competition is still present and leads to a niche shift in the smallest predator of the guild. Interspecific competition may thus be a pervasive force in simple, low productivity food webs characterized by pulsed resources.

La compétition interspécifique peut jouer un rôle clé pour structurer les communautés écologiques. La toundra arctique, un écosystème peu productif, est l'hôte d'un réseau trophique simple où plusieurs prédateurs s'alimentent sur les mêmes proies, les lemmings, connus pour leurs cycles d'abondance de grande amplitude. Nous avons étudié les mécanismes impliqués dans la réduction de la compétition intra-guilde permettant la coexistence de quatre espèces de prédateurs aviaires (harfang des neiges, goéland bourgmestre, buse pattue, labbe à longue queue) qui se nourrissent de ressources fluctuantes (lemmings bruns et variables). Nous avons comparé la taille et les espèces des proies consommées par chaque prédateur afin d'évaluer si une ségrégation se produisait. Nous avons aussi vérifié si une ségrégation spatiale dans les aires de nidification permettait la coexistence de ces prédateurs. Finalement, nous avons testé si l'absence de harfangs, une espèce dominante et irruptive, initiait un relâchement de la compétition sur le plus petit prédateur, le labbe, en changeant la taille de ses proies et de son aire de nidification. Nous avons suivi la reproduction des prédateurs et l'abondance des lemmings pendant 14 ans sur l'Île Bylot (Canada). Nous avons cartographié les nids et récolté des pelotes de régurgitation pour mesurer la taille des mandibules de lemmings et inférer la taille et l'espèce consommées. La taille des lemmings consommés variait selon les espèces, les plus grands prédateurs consommant les plus gros lemmings et le plus petits prédateur les plus petits lemmings. Tous les prédateurs consommaient plus de lemmings variables comparativement à leur disponibilité, bien que les harfangs et les labbes consommaient relativement plus de lemmings bruns que les goélands et les buses. Les labbes ont consommé des lemmings plus gros en l'absence de harfangs qu'en leur présence, suggérant un relâchement de la compétition à court-terme. Nous avons trouvé un chevauchement modéré à faible dans les aires de nidification entre les prédateurs et aucune évidence de leur expansion en l'absence de harfangs. Ceci suggère que la distribution spatiale est causée par les préférences d'habitat de chaque espèce. La ségrégation spatiale constitue le principal mécanisme menant au partage de la ressource alimentaire entre les prédateurs aviaires et, secondairement, la taille et les espèces de proies. Cependant, nous avons trouvé des évidences que la compétition alimentaire est toujours présente et conduit à un changement de la niche chez le plus petit prédateur de la guilde. La compétition interspécifique pourrait donc être une force omniprésente dans les réseaux trophiques simples et peu productifs caractérisés par des ressources fluctuantes.

High Arctic lemmings remain reproductively active under predator-induced elevated stress.

Non-consumptive effects of predation have rarely been assessed in wildlife populations even though their impact could be as important as lethal effects. Reproduction of individuals is one of the most important demographic parameters that could be affected by predator-induced stress, which in turn can have important consequences on population dynamics. We studied non-consumptive effects of predation on the reproductive activity (i.e., mating and fertilization) of a cyclic population of brown lemmings exposed to intense summer predation in the Canadian High Arctic. Lemmings were live-trapped, their reproductive activity (i.e., testes visible in males, pregnancy/lactation in females) assessed, and predators were monitored during the summers of 2014 and 2015 within a 9 ha predator-reduction exclosure delimited by a fence and covered by a net, and on an 11 ha control area. Stress levels were quantified non-invasively with fecal corticosterone metabolites (FCM). We found that FCM levels of lemmings captured outside the predator exclosure (n = 50) were 1.6 times higher than inside (n = 51). The proportion of pregnant/lactating adult females did not differ between the two areas, nor did the proportion of adult scrotal males. We found that lemmings showed physiological stress reactions due to high predation risk, but had no sign of reduced mating activity or fertility. Thus, our results do not support the hypothesis of reproductive suppression by predator-induced stress.

Assessing Stress in Arctic Lemmings: Fecal Metabolite Levels Reflect Plasma Free Corticosterone Levels.

Interest in the ecology of stress in wild populations has triggered the development of noninvasive methods for quantifying stress hormones. Measurement of fecal corticosteroid metabolites (FCMs) is one such method, but it is still unclear whether FCMs can be a reliable proxy of free plasma glucocorticoids. To assess the validity of this assumption, we carried out a robust assessment on brown lemmings (Lemmus trimucronatus) from Bylot Island, Nunavut, Canada, that were hand captured and anesthetized and related plasma glucocorticoid levels to fecal metabolite glucocorticoid levels. We examined endogenous factors that could explain interindividual variability. Blood corticosterone was measured from samples obtained on capture and 30 min later, and FCM levels were measured from animals kept in captivity for 72 h. Plasma free corticosterone increased 135-fold over baseline values 30 min after capture, which confirmed that initial handling was perceived as a stressor. We found that FCM levels were highly related with free (marginal [Formula: see text] = 0.53) but not with total ([Formula: see text] = 0.02) corticosterone levels, regardless of age, sex, and reproductive condition. FCM levels started increasing 2 h after capture and reached maximum levels 4 h after capture. No circadian rhythm in FCMs was found. Plasma total corticosterone levels were much higher in adult females compared with adult males, but this difference was much smaller when measuring free corticosterone levels and FCM levels. Our results suggest that FCM levels are good measures of stress by being closely related to plasma free corticosterone levels in brown lemmings.

Top-down limitation of lemmings revealed by experimental reduction of predators.

It is generally recognized that delayed density-dependence is responsible for cyclic population dynamics. However, it is still uncertain whether a single factor can explain why some rodent populations fluctuate according to a 3-4 yr periodicity. There is increasing evidence that predation may play a role in lemming population cycles, although this effect may vary seasonally. To address this issue, we conducted an experiment where we built a large exclosure (9 ha) to protect brown lemmings (Lemmus trimucronatus) from avian and terrestrial predators. We tested the hypothesis that predation is a limiting factor for lemmings by measuring the demographic consequences of a predator reduction during the growth and peak phases of the cycle. We assessed summer (capture-mark-recapture methods) and winter (winter nest sampling) lemming demography on two grids located on Bylot Island, Nunavut, Canada from 2008 to 2015. The predator exclosure became fully effective in July 2013, allowing us to compare demography between the control and experimental grids before and during the treatment. Lemming abundance, survival and proportion of juveniles were similar between the two grids before the treatment. During the predator-reduction period, summer densities were on average 1.9× higher inside the experimental grid than the control and this effect was greatest for adult females and juveniles (densities 2.4× and 3.4× higher, respectively). Summer survival was 1.6× higher on the experimental grid than the control whereas body mass and proportion of juveniles were also slightly higher. Winter nest densities remained high inside the predator reduction grid following high summer abundance, but declined on the control grid. These results confirm that predation limits lemming population growth during the summer due to its negative impact on survival. However, it is possible that in winter, predation may interact with other factors affecting reproduction and ultimately population cycles.

Seasonal demography of a cyclic lemming population in the Canadian Arctic.

1. The causes of cyclical fluctuations in animal populations remain a controversial topic in ecology. Food limitation and predation are two leading hypotheses to explain small mammal population dynamics in northern environments. We documented the seasonal timing of the decline phases and demographic parameters (survival and reproduction) associated with population changes in lemmings, allowing us to evaluate some predictions from these two hypotheses. 2. We studied the demography of brown lemmings (Lemmus trimucronatus), a species showing 3- to 4-year population cycles in the Canadian Arctic, by combining capture-mark-recapture analysis of summer live-trapping with monitoring of winter nests over a 10-year period. We also examined the effects of some weather variables on survival. 3. We found that population declines after a peak occurred between the summer and winter period and not during the winter. During the summer, population growth was driven by change in survival, but not in fecundity or proportion of juveniles, whereas in winter population growth was driven by changes in late summer and winter reproduction. 4. We did not find evidence for direct density dependence on summer demographic parameters, though our analysis was constrained by the paucity of data during the low phase. Body mass, however, was highest in peak years. 5. Weather effects were detected only in early summer when lemming survival was positively related to snow depth at the onset of melt but negatively related to rainfall. 6. Our results show that high mortality causes population declines of lemmings during summer and fall, which suggests that predation is sufficient to cause population crashes, whereas high winter fecundity is the primary factor leading to population irruptions. The positive association between snow depth and early summer survival may be due to the protective cover offered by snow against predators. It is still unclear why reproduction remains low during the low phase.