Comparing the genetic population structure of two species of arctic lemmings: more local differentiation in Lemmus trimucronatus than in Dicrostonyx groenlandicus

Collared and brown lemmings ( Dicrostonyx groenlandicus and Lemmus trimucronatus ) are two largely sympatric and ecologically comparable species of arctic microtine rodents, differing however in some respects which allow us to hypothesise differences in the genetic structure of their populations. Collared lemmings are particularly well adapted to life at high latitude, they occasionally emerge to the surface of the snow and may disperse over larger distances than brown lemmings – possibly even over snow and ice. This should result in more local differentiation among populations of brown lemmings than among populations of collared lemmings. We compared the genetic population structure between the two lemming species in a fragmented landscape with small islands in the central Canadian Arctic using four microsatellite loci and partial mitochondrial control region sequences. Both types of genetic markers showed higher differentiation ( F _ST values) among local populations for brown lemmings than for collared lemmings. We discuss to what extent the observed genetic differences may be explained by differences in dispersal rates in addition to differences in average effective population size.     

Phylogeography of the circumpolar Paranoplocephala arctica species complex (Cestoda: Anoplocephalidae) parasitizing collared lemmings (Dicrostonyx spp.)

The Paranoplocephla arctica complex (Cyclophyllidea, Anoplocephalidae), host-specific cestodes of collared lemmings Dicrostonyx, include two morphospecies P. arctica and P. alternata, whose taxonomical status now must be considered ambiguous. The genetic population structure and phylogeography of the P. arctica complex was studied from 83 individuals sampled throughout the Holarctic distribution range using 600 bp of the mitochondrial cytochrome c oxidase subunit I gene (COI). The mitochondrial DNA (mtDNA) phylogeny divides the species complex into one main Nearctic and one main Palaearctic phylogroup, corresponding to the main phylogenetic division of the hosts. In the Palearctic phylogroup, the parasite clades correspond to the host clades although the parasites from Wrangel Island form an exception as the host on this island, D. groenlandicus, belongs to the Nearctic phylogroup. In the Nearctic, northern refugia beyond the ice limit of the Pleistocene glaciations are proposed for the hosts. All reconstructions of parasite phylogeny show a genetically differentiated population structure that in the Canadian Arctic lacks strict congruence between phylogeny and geography. The parasite phylogeny does not show complete congruence with host relationships, suggesting a history of colonization and secondary patterns of dispersal from Beringia into the Canadian Arctic, an event not proposed by the host phylogenies alone.     

Photoperiod differentially affects immune function and reproduction in collared lemmings (Dicrostonyx groenlandicus)

Many nontropical rodent species experience predictable annual variation in resource availability and environmental conditions. Individuals of many animal species engage in energetically expensive processes such as breeding during the spring and summer but bias investment toward processes that promote survival such as immune function during the winter. Generally, the suite of responses associated with the changing seasons can be induced by manipulating day length (photoperiod). Collared lemmings (Dicrostonyx groenlandicus) are arvicoline rodents that inhabit parts of northern Canada and Greenland. Despite the extreme conditions of winter in their native habitat, these lemmings routinely breed during the winter. In the laboratory, collared lemmings have divergent responses to photoperiod relative to other seasonally breeding rodents; short day lengths can stimulate, rather than inhibit, the reproductive system. Male and female collared lemmings were maintained for 11 weeks in 1 of 3 photoperiods (LD 22:2, LD 16:8, or LD 8:16) that induce markedly different phenotypes. Following photoperiod treatment, cell-mediated immune function as assessed by delayed-type hypersensitivity reactions was elevated in lemmings housed in LD 16:8 and LD 8:16 relative to LD 22:2. However, antibody production to a novel antigen was unaffected by photoperiod. Exposure to LD 8:16 induced weight gain, molt to a winter pelage, and in contrast to previous studies, regression of the male, but not the female, reproductive tract. In conclusion, these data indicate that components of immune function among collared lemmings are responsive to changes in day length.     

Safety of lyophilized SAG2 oral rabies vaccine in collared lemmings

Fifteen collared lemmings (Dicrostonyx groenlandicus) were exposed to a lyophilized oral rabies vaccine designed to immunize wild carnivore populations. No animals contracted rabies from the vaccine as determined by the absence of clinical signs after 37 days and lack of rabies virus in brain tissue determined by the fluorescent antibody (FA) test. These results suggest that collared lemmings would not contract rabies if they ingested this lyophilized vaccine in the wild during bait vaccination programs for arctic foxes (Alopex lagopus).     

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.     

Phylogeographic structure and mitochondrial DNA variation in true lemmings (Lemmus) from the Eurasian Arctic

The geographic pattern of mtDNA variation in lemmings from 13 localities throughout the Eurasian Arctic was studied by using eight restriction enzymes and sequencing of the cytochrome b region. These data are used to reveal the vicariant history of Lemmus , and to examine the effect of the last glaciation on mtDNA variation by comparing diversity in formerly glaciated areas to the diversity in non-glaciated areas. Phylogenetic congruence across different Arctic taxa and association between observed discontinuities, and probable Pleistocene barriers, suggest that glacial-interglacial periods were crucial in the vicariant history of Lemmus. Differences in amount of divergence (2.1–9.1%) across different historical barriers indicate chronologically separate vicariant events during the Quaternary. Populations from a formerly glaciated area are no less variable than those in the non-glaciated area. Regardless of glaciation history, no population structure and high haplotype diversity were found within geographic regions. The lack of population structure indicates that populations with high ancestral haplotype diversity shifted their distribution during the Holocene, and that lemmings tracked a changing environment during the Quaternary without reduction of effective population size.     

Catechin content and consumption ratio of the collared lemming

Chemical- plant defences as mechanisms affecting herbivore populations have been debated during the past decade. Several authors have questioned the hypothesis, but the present study shows that collared lemmings ( Dicrostonyx groenlandicus) in northeast Greenland prefer food plants with a lower catechin content. Dicrostonyx species are known to have specialised on shrubs, especially Dryas spp. and Salix spp., rather than graminoids like other related microtines. Bioassays were conducted using food material from Dryas spp., Salix arctica, Vaccinium uliginosum, Kobresia myosuroides and Poa glauca. Enclosures with the first three species mentioned were further treated by clipping to simulate herbivory in order to induce the production of the plant defence compound catechin. Treatment increased the catechin content in Dryas spp., S. arctica (females only) and V. uliginosum significantly compared with the catechin concentration in untreated plants. These elevated catechin concentrations had a significantly negative effect on the consumption rate of Dryas spp. and female S. arctica by collared lemmings.     

Multiple glacial refugia in the North American Arctic: inference from phylogeography of the collared lemming (Dicrostonyx groenlandicus)

Cryptic northern refugia beyond the ice limit of the Pleistocene glaciations may have had significant influence on the current pattern of biodiversity in Arctic regions. In order to evaluate whether northern glacial refugia existed in the Canadian Arctic, we examined mitochondrial DNA phylogeography in the northernmost species of rodents, the collared lemming (Dicrostonyx groenlandicus) sampled across its range of distribution in the North American Arctic and Greenland. The division of the collared lemming into the Canadian Arctic and eastern Beringia phylogroups does not support postglacial colonization of the North American Arctic from a single eastern Beringia refugium. Rather, the phylogeographical structure and sparse fossil records indicate that, during the last glaciation, some biologically significant refugia and important sources of postglacial colonization were located to the northwest of the main ice sheet in the Canadian Arctic.     

Spatial structure of lemming populations (Dicrostonyx groenlandicus) fluctuating in density

The pattern and scale of the genetic structure of populations provides valuable information for the understanding of the spatial ecology of populations, including the spatial aspects of density fluctuations. In the present paper, the genetic structure of periodically fluctuating lemmings (Dicrostonyx groenlandicus) in the Canadian Arctic was analysed using mitochondrial DNA (mtDNA) control region sequences and four nuclear microsatellite loci. Low genetic variability was found in mtDNA, while microsatellite loci were highly variable in all localities, including localities on isolated small islands. For both genetic markers the genetic differentiation was clear among geographical regions but weaker among localities within regions. Such a pattern implies gene flow within regions. Based on theoretical calculations and population census data from a snap-trapping survey, we argue that the observed genetic variability on small islands and the low level of differentiation among these islands cannot be explained without invoking long distance dispersal of lemmings over the sea ice. Such dispersal is unlikely to occur only during population density peaks.     

Cytogenetics of collared lemmings (Dicrostonyx groenlandicus). II. Meiotic behavior of B chromosomes suggests a Y-chromosome origin of supernumerary chromosomes

The patterns of synapsis and chiasma formation of the B chromosomes of male collared lemmings (Dicrostonyx groenlandicus) were analyzed by light and electron microscopy and compared to expectations for various hypotheses for the intragenomic origin of supernumerary chromosomes. Pachytene analysis revealed a variety of synaptic configurations including B-chromosome univalents, bivalents and trivalents. In approximately one-half of the pachytene nuclei examined, B chromosomes were in synaptic associations with the normally unpaired portion of the Y chromosome. The B-chromosome configurations at pachynema, including those involving the Y chromosome, were maintained into diakinesis and metaphase I. The meiotic behavior of the B chromosomes was inconsistent with their derivation from centric-fusion products, isochromosome formation, small-autosome polysomy, or the X chromosome. However, the frequent synapsis and apparent recombination between B chromosomes and the Y chromosome implicate this sex chromosome as a possible source of the B chromosomes in collared lemmings.     

Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late Quaternary biogeography of high latitudes

A species-wide phylogeographical study of the root vole (Microtus oeconomus) was performed using the whole 1140 base pair mitochondrial (mt) cytochrome b gene. We examined 83 specimens from 52 localities resulting in 65 unique haplotypes. Our results demonstrate that the root vole is divided into four main mtDNA phylogenetic lineages that seem to have largely allopatric distributions. Net divergence estimates (2.0-3.5%) between phylogroups, as well as relatively high nucleotide diversity estimates within phylogroups, indicate that the distinct phylogeographical structure was initiated by historical events that predated the latest glaciation. European root voles are divided into a Northern and a Central mtDNA phylogroup. The mtDNA data in concert with fossil records imply that root voles remained north of the classical refugial areas in southern Europe during the last glacial period. The currently fragmented populations in central Europe belong to a single mtDNA phylogroup. The Central Asian and the North European lineages are separated by the Ural Mountains, a phylogeographical split also found in collared lemmings (Dicrostonyx) and the common vole (M. arvalis). The Beringian lineage occurs from eastern Russia through Alaska to northwestern Canada. This distribution is congruent with the traditional boundaries of the Beringian refugium and with phylogeographical work on other organisms. In conclusion, similarities between the phylogeographical patterns in the root vole and other rodents, such as Arctic and subarctic lemmings, as well as more temperate vole species, indicate that late Quaternary geological and climatic events played a strong role in structuring northern biotic communities.     

Metabolic rate and thermal conductance of lemmings from high-arctic Canada and Siberia

The arctic climate places high demands on the energy metabolism of its inhabitants. We measured resting (RMR) and basal metabolic rates (BMR), body temperatures, and dry and wet thermal conductances in summer morphs of the lemmings Dicrostonyx groenlandicus and Lemmus trimucronatus in arctic Canada, and the BMR of D. torquatus, D. groenlandicus, L. sibiricus, L. bungei and L. trimucronatus in Siberia. In contrast to previous studies the data were collected on animals that had spent only a limited time in captivity. All parameters were analysed in relation to the variations in body mass (20-90 g). Body temperature and BMR were lower in D. groenlandicus than L. trimucronatus, which coincides with greater longevity in the former species. Wet and dry thermal conductances of both species were similar and comparable with those of other Myomorpha (mouse-type rodents), indicating no evidence for a previously claimed lower thermal conductance in lemmings. BMR in lemmings appeared to be higher than in other Arvicolidae (voles, lemmings and muskrats), which could relate to their typically high-latitude distribution. However, the more southerly living Lemmus species had higher BMR than the more northerly living Dicrostonyx species, which may be explained by the former having a relatively low-quality diet.     

The influence of photoperiod on growth and sexual function in male and female collared lemmings (Dicrostonyx groenlandicus).

The effect of photoperiod on sexual function and growth in weanling male and female collared lemmings (Dicrostonyx groenlandicus) was studied. Males and females maintained in 6 hr light:18 hr dark after weaning were larger at the end of 70 days than their siblings kept in 20L:4D. Males in 6L:18D were longer and overall body growth was greater. Males in 6L:18D had heavier adrenals but there were no differences in the weights of testes, preputial glands or seminal vesicles or in the mean testosterone levels of the two groups. Females in 6L:18D had heavier preputial glands than the 20L:4D females. There were no differences between the two groups in uterine, ovarian or adrenal weights or in the number or mean size of atretic or healthy Graafian follicles. Adult males kept in 6L:18D increased more in body weight than those in 20L:4D, but there was no detectable influence of the short photoperiod on reproductive function.     

Variations of skull-body regressions of the lemming (Dicrostonyx groenlandicus) under laboratory and field conditions

Collared lemmings, Dicrostonyx groenlandicus , maintained in the laboratory under short-day photoperiods (2 h light: 22 h dark) grew faster than their cohorts kept under long-day photoperiods (22 h light: 2 h dark). Significant differences in cranial, visceral and body components were found in both sexes. Linear regressions of skull-body parameters were compared to those of wild lemmings trapped at Eskimo Point, Northwest Territories, Canada, during three consecutive summers from 1973 to 1975. The data support the conclusion that variation in body size and skull development associated with changes in population density are, in part, due to photoperiod influences. The importance of this facultative response is discussed in relation to current theories on thermal regulation and variations in subnivial breeding success observed in this species.     

The summer decline of the collared lemming, Dicrostonyx groenlandicus, in high arctic Greenland

I studied the population structure and dynamics of the collared lemming, Dicrostonyx groenlandicus Traill, on Traill Island (NE Greenland) in 1998 to 2000. This is the first comprehensive study of a Greenlandic collared lemming population. During this period, population density continuously declined (>100 fold-decrease) from more than 10 ind/ha (peak year 1998) to less than 0.1 ind/ha (low year 2000), with the exception of one period of increase in the winter 1998–99. Several population parameters were correlated with these changes in density. Average body mass was greater in the peak year than in the intermediate year (1999) and greater in August than in July in both years. Growth rates were only positive in 1998 and only for young lemmings. Females had unexpectedly larger home ranges than males and were more mobile than males during the decline phase (1999). Poor recruitment and high predation rates (up to 3.4% per day for females in 1998) were the proximate causes of the summer declines in the study area. A simple calculation shows that even with a maximal rate of increase, this lemming population would not have been able to compensate for the high predation rate, and hence it necessarily faced a predation-induced summer decline during the part of population oscillation studied.     

Demography of two lemming species on Bylot Island, Nunavut, Canada

Lemmings play a key role in the tundra food web and their widely reported cyclic oscillations in abundance may have a strong effect on other components of the ecosystem. We documented seasonal and annual variations in population density, reproductive activity, survival, and body mass of two sympatric species, the brown (Lemmus trimucronatus) and collared lemmings (Dicrostonyx groenlandicus), over a 2-year period on Bylot Island, Nunavut, Canada. We live trapped and marked lemmings on two grids throughout the summer and we estimated demographic parameters using three different capture–recapture methods. All three methods are based on robust estimators and they yielded similar population density estimates. The density of brown lemmings declined markedly between the 2 years whereas that of collared lemmings was relatively constant. For brown lemmings, 2004 was a peak year in their cycle and 2005 a decline phase. Density of brown lemmings also decreased during the summer, but not that of collared lemmings. The recruitment of juvenile brown lemmings in the population increased during the summer and was higher in the peak year than in the year after, but no change was detected in collared lemmings. Survival rates of both species tended to be lower during the peak year than in the following year and body mass of brown lemmings was higher in the peak year than in the following year. We conclude that both changes in adult survival and juvenile recruitment occur during the population decline of brown lemmings.     

Habitat use by lemmings near Barrow, Alaska

Brown lemmings reach much higher densities than collared lemmings near Barrow, Alaska, and captures from 19 summers of snap trapping confirm previous reports that brown lemmings prefer lower, wetter habitats than do collared lemmings. Data also support the hypothesis that brown lemmings concentrate in higher habitats during early summer when melt water floods lower habitats, then shift to lower habitats where preferred food is more available as the waters recede. This pattern appears similar to seasonal shifts in habitat use reported for Norwegian lemmings. Two hypotheses were not supported by our data: (1) Unlike Norwegian lemmings, brown lemmings did not expand their use of suboptimal habitats at higher population densities. Rather, absolute densities changed in concert so that the relative densities among habitats remained unchanged. (2) Preferential use of polygon troughs during winter, as indicated by patterns of winter grazing, was not simply a function of snow depth. Instead it appeared to be related to shoot density of preferred foods. Nearly all patterns of habitat use seemed to be linked to food availability. Other factors, such as protection from predators by vegetative cover in summer and increased insulation from deeper snow in winter, did not appear to influence the distribution of lemmings as strongly.     

Landscapes of fear or competition? Predation did not alter habitat choice by Arctic rodents

In systems where predation plays a key role in the dynamics of prey populations, such as in Arctic rodents, it is reasonable to assume that differential patterns of habitat use by prey species represent adaptive responses to spatial variation in predation. However, habitat selection by collared (Dicrostonyx groenlandicus) and brown (Lemmus trimucronatus) lemmings depends on intra- and inter-specific densities, and there has been little agreement on the respective influences of food abundance, predators, and competition for habitat on lemming dynamics. Thus, we investigated whether predation affected selection of sedge-meadow versus upland tundra by collared lemmings in the central Canadian Arctic. We first controlled for the effects of competition on lemming habitat selection. We then searched for an additional signal of predation by comparing habitat selection patterns between 12 control plots and one large grid where lemmings were protected from predators by fencing in 1996 and 1997, but not during 5 subsequent years when we monitored habitat use in the grid as well as in the control plots. Dicrostonyx used upland preferentially over meadows and was more numerous in 1996 and 2011 than in other sample years. Lemmus was also more abundant in 1996 than in subsequent years, but its abundance was too low in the exclosure to assess whether exclusion of predators influenced its habitat selection. Contrary to the effects of competition, predation had a negligible impact on the spatial dynamics of Dicrostonyx, at least during summer. These results suggest that any differences in predation risk between the two habitats have little direct influence on the temporal dynamics of Dicrostonyx even if induced through predator–prey cycles.