Lemmus Trimucronatus Research Articles

Benefiting from a migratory prey: spatio‐temporal patterns in allochthonous subsidization of an arctic predator

1. Flows of nutrients and energy across ecosystem boundaries have the potential to subsidize consumer populations and modify the dynamics of food webs, but how spatio-temporal variations in autochthonous and allochthonous resources affect consumers' subsidization remains largely unexplored. 2. We studied spatio-temporal patterns in the allochthonous subsidization of a predator living in a relatively simple ecosystem. We worked on Bylot Island (Nunavut, Canada), where arctic foxes (Vulpes lagopus L.) feed preferentially on lemmings (Lemmus trimucronatus and Dicrostonyx groenlandicus Traill), and alternatively on colonial greater snow geese (Anser caerulescens atlanticus L.). Geese migrate annually from their wintering grounds (where they feed on farmlands and marshes) to the Canadian Arctic, thus generating a strong flow of nutrients and energy across ecosystem boundaries. 3. We examined the influence of spatial variations in availability of geese on the diet of fox cubs (2003-2005) and on fox reproductive output (1996-2005) during different phases of the lemming cycle. 4. Using stable isotope analysis and a simple statistical routine developed to analyse the outputs of a multisource mixing model (SIAR), we showed that the contribution of geese to the diet of arctic fox cubs decreased with distance from the goose colony. 5. The probability that a den was used for reproduction by foxes decreased with distance from the subsidized goose colony and increased with lemming abundance. When lemmings were highly abundant, the effect of distance from the colony disappeared. The goose colony thus generated a spatial patterning of reproduction probability of foxes, while the lemming cycle generated a strong temporal variation of reproduction probability of foxes. 6. This study shows how the input of energy owing to the large-scale migration of prey affects the functional and reproductive responses of an opportunistic consumer, and how this input is spatially and temporally modulated through the foraging behaviour of the consumer. Thus, perspectives of both landscape and foraging ecology are needed to fully resolve the effects of subsidies on animal demographic processes and population dynamics.

A redescription of Arostrilepis beringiensis (Kontrimavichus et Smirnova, 1991) and descriptions of two new species from Palaearctic microtine rodents, Arostrilepis intermedia sp. n. and A. janickii sp. n. (Cestoda: Hymenolepididae)

Arostrilepis beringiensis (Kontrimavichus et Smirnova, 1991) is redescribed on the basis of its type specimens from Lemmus trimucronatus (Richardson) and material from the collections of the Institute of Systematics and Ecology of Animals, Novosibirsk from the lemmings Myopus schisticolor (Lilljeborg) and Lemmus sibiricus (Kerr) from the Asian part of Russia. Specimens previously identified as Arostrilepis horrida (Linstow, 1901) from voles are revised and newly collected materials are addressed. Two new species of the genus Arostrilepis Mas-Coma et Tenora, 1997, A. intermedia sp. n. from red-backed voles (Myodes Pallas) from the Asian part of Russia and A. janickii sp. n. from Europe, are described. These species are clearly distinguished from congeners by form and size of the cirrus and its armature as well as the type of arrangement for the testes, position of the cirrus-sac with regard to poral ventral osmoregulatory canals, and host specificity.

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.

Evaluation of a method to determine the breeding activity of lemmings in their winter nests

Winter breeding under the snow is a critical ecological adaptation of lemmings and a key demographic process in their periodic multiannual fluctuations in abundance. However, logistic constraints limit our ability to quantify lemming winter reproduction. We evaluated a method to infer lemming reproduction based on the size distribution of feces found in their winter nests. We determined criteria allowing identification of reproduction from feces found in nests, using golden Syrian hamsters (Mesocricetus auratus) as a surrogate model. We found a large difference in individual mass of feces between juveniles at weaning and adults. Using bimodal distribution of feces size, mean size difference, and proportion of small feces, we showed that visual inspection of ≥30 feces was sufficient to infer hamster reproduction with an accuracy of >95%. We also applied the method to winter nests of collared lemmings (Dicrostonyx groenlandicus) and brown lemmings (Lemmus trimucronatus) found in the Canadian Arctic. Because characteristics of feces found in lemming winter nests matched those found in hamster nests, we suggest that the method can be used to detect winter reproductive activity of lemmings.

Forecasting ecological and evolutionary strategies to global change: an example from habitat selection by lemmings

Ecologists and evolutionary biologists must develop theories that can predict the consequences of global warming and other impacts on Earth's biota. Theories of adaptive habitat selection are particularly promising because they link distribution and density with fitness. The evolutionarily stable strategy that emerges from adaptive habitat choice is given by the system's habitat isodar, the graph of densities in pairs of habitats such that the expectation of fitness is the same in each. We illustrate how isodars can be converted into adaptive landscapes of habitat selection that display the density- and frequency-dependent fitness of competing strategies of habitat use. The adaptive landscape varies with the abundance of habitats and can thus be used to predict future adaptive distributions of individuals under competing scenarios of habitat change. Application of the theory to three species of Arctic rodents living on Herschel Island in the Beaufort Sea predicts changes in selection gradients as xeric upland increases in frequency with global warming. Selection gradients will become more shallow for brown lemming (Lemmus trimucronatus) and tundra vole (Microtus oeconomus) strategies that preferentially exploit mesic habitat. Climate change will cause selection gradients for the alternative strategy of using mostly xeric habitat to become much steeper. Meanwhile, the adaptive landscape for collared lemmings (Dicrostonyx groenlandicus), which specialize on xeric Dryas-covered upland, will become increasingly convex. Changes in the adaptive landscapes thus predict expanding niches for Lemmus and Microtus, and a narrower niche for Dicrostonyx. The ability to draw adaptive landscapes from current patterns of distribution represents one of the few methods available to forecast the consequences of climate change on the future distribution and evolution of affected species.

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.

Seasonal glucocorticoid responses to capture in wild free-living mammals

We determined baseline and capture-induced glucocorticoid concentrations during two different seasons in three species of wild free-living rodents: brown lemmings (Lemmus trimucronatus), golden-mantled ground squirrels (Spermophilus saturatus), and yellow-pine chipmunks (Tamias amoenus). Initial blood samples were obtained within 3 min of capture, so that initial glucocorticoid levels reflect baseline titers of undisturbed animals. Animals were held for an additional 30 min, when a second blood sample was taken to measure stress-induced glucocorticoid titers. The primary glucocorticoid differed in each species. Lemmings secreted extremely large amounts of corticosterone (as high as 8,000 ng/ml). These high concentrations were accompanied by high corticosterone-binding globulin capacity and resistance to negative feedback. Squirrels and chipmunks secreted a mixture of cortisol and corticosterone (10-400 ng/ml). In males of all three species and female squirrels and chipmunks, glucocorticoid levels were significantly elevated 30 min after capture. Baseline and 30-min glucocorticoid levels differed seasonally in each species. Levels were higher during summer (with no snow cover) than in spring (with approximately 60% snow cover) in female lemmings, higher during breeding than before hibernation in squirrels, and higher postreproductively than during breeding in chipmunks. Together, these data indicate that glucocorticoid responses to stress in these free-living species are similar to those in laboratory species, but the magnitude of the response appears to depend on life-history features specific to each species.

OCCURRENCE AND DISTRIBUTION OF SMALL MAMMALS ON THE GOODNEWS RIVER, SOUTHWESTERN ALASKA

A paucity of data exists on the occurrence, distribution, and abundance of small mammal communities in southwestern Alaska. To add to the understanding of these communities we conducted a comprehensive small mammal survey in southwestern Alaska. We trapped small mammals along the Goodnews River in Togiak National Wildlife Refuge from 26 June to 5 September 1996. Objectives of our study were to determine what small mammal species occur in the Goodnews River area, to determine species distribution in 4 representative habitats during 3 time periods, and to determine ideal time periods to trap small mammals in order to maximize the diversity of species encountered and the number of specimens captured. In 3600 trap-nights we captured 468 specimens including masked shrew (Sorex cinereus), pygmy shrew (S. hoyi), Alaska tiny shrew (S. yukonicus), tundra shrew (S. tundrensis), tundra vole (Microtus oeconomus), red-backed vole (Clethrionomys rutilus), Greenland collared lemming (Dicrostonyx groenlandicus), and brown lemming (Lemmus trimucronatus). The pygmy shrew, Alaska tiny shrew, Greenland collared lemming, and brown lemming are the 1st representatives of these species from the region to be placed in a museum collection. The willow habitat supported the greatest number of specimens captured (n = 170), while the wet tundra habitat yielded the greatest number of species captured (n = 4). The fall trap period (26 August to 5 September) yielded the greatest number of specimens captured (n = 229), while the spring (26 June to 6 July) and summer trap periods (26 July to 5 August) yielded greatest species diversity. Findings of rare and uncommon species illustrate the need to conduct additional surveys in the region.

Significant Morphological but Little Molecular Differences Between Trypanosoma of Rodents From Alaska

We examined blood smears of 173 rodents and 33 shrews captured at 4 sites in the Gates of the Arctic National Park, northern Alaska, in summer 2002. Trypanosoma spp. were detected in the plasma of 5 Microtus oeconomus, 4 Microtus miurus, and 1 Lemmus trimucronatus. The trypomastigote morphology from different individuals of M. oeconomus caught at the same site and of M. miurus from different sites varied significantly. The 4 DNA sequences obtained from the blood smear positive samples contained 2 different haplotypes very similar to each other and to that of Trypanosoma microti. Of possible vectors of blood parasites, the flea Amalaraeus dissimilis was collected from M. miurus.

New Distribution Records of Echinococcus multilocularis in the Brown Lemming from Barrow, Alaska, USA

We identified Echinococcus multilocularis for the first time in brown lemmings (Lemmus trimucronatus) from Barrow, Alaska, USA. Of 467 brown lemmings trapped between 1995 and 2000, two males and two females (0.9%; 95% confidence interval=0.9+/-0.9%) were found to be infected with metacestodes of E. multilocularis. No metacestodes were found in 17 collared lemmings (Dicrostonyx rubricatus) also trapped at Barrow. In humans, E. multilocularis causes alveolar echinococcosis, which is potentially fatal. Knowledge of the distribution of this parasite is important to protect the public health.

Intraclonal variation in defence substances and palatability: a study on Carex and lemmings

Clonal sedges consist of integrated ramets at different development stages. Many of these sedges are important food for herbivores, yet differences in herbivore preferences and defence allocation between ramet development stages have not previously been evaluated. In this study we investigated intraclonal ramet variation in level of plant defence and nutrient compounds and intraclonal ramet preferences by lemmings (Lemmus trimucronatus) in field samples of a rhizomatous sedge (Carex stans). Plant defence was measured as the level of proteinase inhibitor activity (PIA) and the ratio of PIA to soluble plant proteins (SPP), whereas plant nutrients were measured as the level of soluble plant sugars (SPS) and SPP. Flowering ramets generally had a higher content of defence compared to vegetative ramets, which is consistent with the optimal defence theory predicting that defence compounds are allocated to the ramet stage of the highest fitness value. Compared to vegetative ramets, the flowering ramets had a lower content of SPP and a higher content of SPS. The lemmings showed preference differences between the ramet development stages, and to a large extent the ramet content of defence compounds and nutrient compounds covaried with these preferences in the predicted way. This study shows that defence allocation between ramet development stages of the clonal sedge Carex conforms to predictions of the optimal defence theory.

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.

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 (FST 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.

Limit cycles in Norwegian lemmings: tensions between phase–dependence and density-dependence

Ever since Elton, the 3–5 year density cycles in lemmings (and other microtines) in Fennoscandia have troubled scientists. Explanations have involved intrinsic regulation and trophic interactions. We have analysed yearly changes in fall abundances for lemmings over 25 years from two local mountain sites in South Norway. These time series appear to have an underlying nonlinear structure of order two. Fitting a piece-wise linear threshold model of maximum order two, the most parsimonious model was, however, of first order for both series. The resulting dynamics from this model is a limit cycle. Reformulating the model in terms of abundances yields a model which combines (delayed) density-dependent effects and the influence of the cyclic phase. The delayed density-dependence of one part of the model is consistent with an effect of specialist predators during the peak and crash phases of the cycle, although other trophic interactions cannot be excluded.

Differential attraction of females to dominant males: Olfactory discrimination and mating preference in the brown lemming (Lemmus trimucronatus)

This study investigated differential attraction of estrous brown lemmings (Lemmus trimucronatus) to conspecific males recently exposed to each other for a 10-min agonistic encounter. In tests conducted 5 min, 1 h and 24 h after agonistic encounters, females preferred the oder of dominant males to that of defeated males when both odors were presented simultaneously in a Y-maze olfactometer. Defeat in an agonistic encounter did not reduce the propensity of male lemmings to initiate sexual behavior. In one-male, one-female tests conducted 5 min after agonistic encounters, dominant males achieved higher mount and thrust scores while defeated males obtained higher scores for attempted mounts. The sexual behavior of dominant and defeated males did not differ significantly in similar tests conducted 1 h and 24 h later. In contrast, females readily mated with dominant males and tended to avoid defeated males in two-male tethering tests conducted 5 min after agonistic encounters. In these tests, females still showed a preference for dominant males 1 h and 24 h after male agonistic encounters.

Male dominance status, female choice and mating success in the brown lemming, Lemmus trimucronatus

The objective of this study was to determine whether female brown lemmings would selectively mate with dominant conspecific males. In dyadic encounters, oestrous females paired with dominant males engaged in more frequent lordosis and contact social behaviours than those paired with subordinate males. However, the mount and thrust scores of dominant and subordinate males did not differ significantly. When females had simultaneous access to tethered dominant and subordinate males, they spent more time in close proximity to dominant males and avoided contact with subordinate males. Copulation scores were higher with dominant males. In triadic encounters with free-moving dominant and subordinate males, oestrous females spent more time near, and engaged in more sexual behaviour with, dominant males. Intermale agonistic interactions resulted in ‘privileged access’ to females by dominant males. Sexual behaviour scores were lower and there was a 10-fold increase in intermale aggression in triadic encounters between females and unfamiliar dominant and subordinate males. Both intermale agonistic interactions and female ‘choice’ behaviour accounted for the differential copulatory success of dominant males.

Natural or hormone-induced sexual and social behaviors in the female brown lemming ( Lemmus trimucronatus)

The behaviors of intact or ovariectomized, estradiol benzoate-treated or estradiol benzoate followed by progesterone-treated female brown lemmings were compared. Intact, diestrous females engaged in more social interactions with a male than did ovariectomized females (Experiment 1). In the first 5 min of a 1-hr mating exposure (Experiment 2, Test A) intact females in natural estrus engaged in more social and sexual behaviors than did ovariectomized females in estrogen-induced estrus. However, during the last 5 min of the 1-hr exposure (Test B) ovariectomized females receiving estrogen alone continued to show high levels of sexual activity with a male partner, while intact estrous females or females receiving estrogen followed by progesterone showed an apparent drop in sexual receptivity and an increase in aggressivity. Aggressive behaviors, as indexed by threat-leap behaviors on the part of the female may increase in the presence of progesterone. Declines in sexual activity, occurring within 1 hr of progesterone injection, were apparently dependent on the interaction of progesterone and copulatory events which may affect both the male and female.

The effects of cross-fostering on the behaviour of two species of North American lemmings, Dicrostonyx groenlandicus and Lemmus trimucronatus: I. Olfactory preferences

To determine the role of the maternal environment in the development of adult olfactory preferences, the young of two species of North American lemmings ( Dicrostonyx groenlandicus and Lemmus trimucronatus) were reciprocally cross-fostered shortly after birth. In-fostered (reared by foster conspecific females) and non-fostered animals served as controls. When adult, subjects were tested for olfactory preferences in a free-choice Y-maze olfactometer. When compared to controls, cross-fostered animals showed increased preference for heterospecific odour. This effect was stronger for males than for females. These results suggest that adult species-specific odour preferences are learned during the neonatal period.

The effects of cross-fostering on the behaviour of two species of North American lemmings, dicrostonyx groenlandicus and lemmus trimucronatus: II. Sexual behaviour

The role of the maternal environment in development of sexual behaviour was investigated by reciprocally cross-fostering two species of lemmings ( Dicrostonyx groenlandicus and Lemmus trimucronatus). Non-fostered and within-species-fostered animals served as controls. When adult, cross-fostered (CF) animals engaged in more contact social and sexual behaviours with the foster species than did controls. Lemmings reared by conspecific dams directed sexual behaviour exclusively toward conspecifics. Since CF animals also mated with conspecifics, cross-fostering appears to have resulted in a broadening of ‘species identity’ to include the foster species. These results suggest that neonatal learning of the species characteristics of the mother is important in the ontogeny of premating sexual isolation in these species.

Food Habits, Energetics, and the Population Biology of Mammals

Data presented in this paper suggest that a complex interaction occurs between the physiological parameters of mammals and the growth and fluctuation of their populations: The Malthusian parameter rm increases with rate of metabolism, which in turn varies with body size and food habits. It can be concluded that it behooves all mammals to have as high a rate of metabolism as can be sustained by the quantity and quality of their food resources in space and time, because this adjustment will permit them to maximize their reproductive efforts. These interactions raise many questions, one of which concerns the temporal variation in reproductive strategies. Thus, Coady (1975) showed that the basal rate in the brown lemming (Lemmus trimucronatus) may be especially high during a winter in which the snow cover is reduced. Does a seasonal variation in the rate of metabolism therefore have a significant influence on seasonal variation in reproduction and therefore in population size? Whatever the correct answer to t...