Endocrine Correlates of Seasonal Body Mass Dynamics in the Collared Lemming (Dicrostonyx groenlandicus)

Many winter-active temperate rodent species show seasonal, photoperiod-mediatedchanges in body mass that correlate with changes in food availability,gaining mass when food is abundant. The collared lemming (Dicrostonyxgroenlandicus), an arctic species, also undergoes a seasonaltransition in body mass, but one that is temporally out of phasewith that observed in species from lower latitudes; whereastemperate species increase in mass when exposed to relativelylong day lengths, collared lemmings do so under long but decreasingday lengths. This adaptation may be in response tothe timingof peak above-ground biomass in the arctic. Validation of thishypothesis requires a more thorough examination of both collaredlemmings and other arctic species. In the collared lemming, photoperiod-mediated changes in bodymass are correlated with changes in serum concentrations ofprolactin, thyroid hormones, corticosterone, and growth hormone,and pineal concentrations of melatonin. These observations arecompared to those obtained with temperate small mammals, andpossible cause-and-effect relationships between body mass andhormonal parameters are discussed.     

Effects of Energy Expenditure and Ucp1 on Photoperiod‐Induced Weight Gain in Collared Lemmings

Objective: To determine the role of total energy expenditure (TEE) and its components in the ability of collared lemmings to increase weight in response to a decrease in photoperiod. Research Methods and Procedures: Energy expenditure was measured by 24‐hour indirect calorimetry concurrent with food‐intake studies. TEE and resting and nonresting energy expenditure (REE and NREE, respectively) were adjusted for body weight by analysis of covariance (ANCOVA). Uncoupling protein 1 (Ucp1) mRNA levels from interscapular brown adipose tissue were determined by Northern blot. Results: TEE and REE of lemmings exposed to a short photoperiod for 10 days were significantly lower than that of lemmings exposed to a long photoperiod (p < 0.05), whereas NREE was not significantly different (p = 0.44). Ucp1 mRNA levels in interscapular brown adipose tissue were 50% lower in short‐ vs. long‐photoperiod lemmings (p < 0.01). Ucp1 mRNA levels were positively related to REE (r² = 0.79, p < 0.01). After adjustment of REE for differences in Ucp1 mRNA levels, there was no longer a significant difference attributable to photoperiod treatment (p = 0.54). Discussion: The results of this study indicate that the increase in body mass that occurs when collared lemmings are exposed to a short photoperiod may be primarily fueled by a decrease in REE and is correlated with a decrease in Ucp1 mRNA levels.     

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.     

Population dynamics of the collared lemming and the tundra vole at Pearce Point,Northwest Territories,Canada

From 1987 to 1989 we monitored population changes during summer of the collared lemming (Dicrostonyx groenlandicus) and the tundra vole (Microtus oeconomus) at Pearce Point, Northwest Territories, Canada (69° 48 N, 122° 40 W). Populations on four study areas did not cycle but remained at low density (<3/ha) each year and continued at low numbers for the following 3 years (Reid et al. 1995). Lemming numbers often declined throghout the summer in spite of continous reproduction, and population recovery occurred overwinter. Heavy predation losses of radio-collared lemmings occurred each summer and this lemming population may be trapped in a predator-pit. Collared lemmings breed in winter and only because of winter population growth do these populations persist. Tundra vole numbers increased rapidly in most summers but usually declined overwinter. Tundra voles do not seem able to sustain winter reproduction in this extreme environment and this prevents them from reaching high density because of the short summer. Population growth in both these rodents could be prevented by poor food or by predation losses, and landscape patchiness may also help to prevent population growth. For lemmings we do not think that a shortage of shelter or intrinsic limitations could be restricting population increase at Pearce Point. This is the first detailed study of a non-cyclic collared lemming population.     

Does lemming winter grazing impact vegetation in the Canadian Arctic?

In low-productivity environments such as the tundra, it has been proposed that regular, multi-annual population cycles of lemmings could be driven by winter food depletion in years of peak abundance. If lemming population dynamics is controlled by food resources, we predict that (1) winter grazing should negatively impact the abundance of food plants, (2) this impact should be proportional to lemming density and (3) high lemming winter grazing pressure should result in reduced plant growth during the following summer. We tested these predictions on Bylot Island, Nunavut, Canada, where two species of lemmings are present: the brown (Lemmus trimucronatus) and collared lemming (Dicrostonyx groenlandicus). We installed 16 exclosures in their preferred wintering habitat (snowbeds) and annually sampled plant biomass inside and outside exclosures at snow melt and at peak growth during the summers of 2009–2012, covering a full population cycle. Winter grazing had no impact on total vascular plant or moss biomass at snow melt in all years. Among plant families, only Caryophyllaceae, which was uncommon, showed a decline. In moss taxa, a negative effect was found on Polytrichum in only 1 year out of three. Overall, plant regrowth during the subsequent summer showed annual variation and tended to be reduced in the 2 years of high lemming abundance. However, this could be a consequence of summer grazing. Overall, the impact of lemming winter grazing on plants was weak and short-lived, even in years of high lemming abundance. Therefore, our results are not consistent with the hypothesis that food depletion during winter was the cause of the lemming decline following peak abundance at our study site. Other factors may limit lemming populations and prevent them from reaching densities high enough to exhaust their food resources.     

Body Composition in a Seasonal Model of Obesity: Longitudinal Measures and Validation of DXA

Objective: Collared lemmings, Dicrostonyx groenlandicus, show rapid changes in body mass on a seasonal basis. The objective of this study was to measure longitudinal changes in body composition in animals undergoing photoperiod-induced weight gain and loss using DXA. Research Methods and Procedures: Adult, female collared lemmings exposed to either long (LD; 22 hours light/2 hours dark) or short (SD; 8 hours light/16 hours dark) photoperiods were anesthetized, and DXA was used to determine fat mass, lean tissue mass (LTM), total-body bone mineral content, and total-bone mineral density. After a baseline scan, one-half of the animals were transferred to the alternate photoperiod (SD-LD, weight loss; LD-SD, weight gain) and one-half remained on the same photoperiod (controls; SD-SD, LD-LD). Body composition was determined by DXA after 4 and 8 weeks. Animals were killed, and body composition was determined by carcass analysis. DXA-derived data were validated by comparing with carcass analysis. Results: Body composition by DXA was highly related to body composition measured by chemical analysis, thereby justifying the use of DXA. Lemmings in the SD-LD group lost weight, and this was reflected in measurable losses of fat and LTM. Lemmings in the LD-SD group gained weight, which was shown by measurable increases in fat, LTM and total-body bone mineral content. Discussion: Comparison of body composition determined by DXA to that by chemical extraction revealed that DXA is useful for measuring body composition. The longitudinal analysis revealed that collared lemmings undergo rapid changes in body composition when exposed to changes in photoperiod.     

Functional and numerical responses of four lemming predators in high arctic Greenland

The high‐arctic tundra ecosystem has the world's simplest vertebrate predator–prey community, with only four predators preying upon one rodent species, the collared lemming (Dicrostonyx groenlandicus). We document the functional and numerical responses of all the four predators in NE Greenland. Using these data, we assess the impact of predation on the dynamics of the collared lemming with a 4 yr cycle and >100‐fold difference between maximum and minimum densities. All predator species feed mostly (>90%) on lemmings when lemming density is >1 ha^?1, but the shapes of the predators’ responses vary greatly. The snowy owl (Nyctea scandiaca) is present and breeds only when lemming densities at snowmelt are >2 ha^?1, giving rise to a step‐like numerical response. The long‐tailed skua (Stercorarius longicaudus) has a type III functional response and shifts from alternate food (mainly berries and insects) to lemmings with increasing lemming density. The skua surpasses all the other predators in summer by its total response. The type III functional response of the Arctic fox (Alopex lagopus) starts to increase at much lower lemming densities than the responses of the avian predators, but it has only a weak numerical response. Finally, the stoat (Mustela erminea) is the most specialized predator and the only one with a clearly delayed numerical response. According to their specific functional and numerical responses, each predator plays a key role at some point of the lemming cycle, but only the stoat has the potential to drive the lemming cycle. Stoat predation is greatly reduced in the winter preceding the lemming peak, and it reaches a maximum in the winter preceding the lowest lemming summer density. Stoat predation appears to maintain low lemming densities for at least two successive years. Our study provides empirical support for the specialist predator hypothesis about small mammal population cycles.     

The topography of Gomori positive neurosecretory elements of the hypothalamus of the lemmings Dicrostonyx torquatus and Lemmus sibiricus]

Under study was the structure of the hypothalamo-hypophyseal neurosecretory system in two species of lemmings of the Wrangel island: the collared lemming, (Dicrostonyx torquatus) and the Ob lemming (Lemmus sibiricus). Inspite of the similarity in the general organization of this system in all rodents, certain species features were found in the topography of neurosecretory elements in the animals studied. In the Ob lemming there is a great similarity in the structures of the neurosecretory system with the albino rat than in the collared lemming. In both species of lemmings, and in the collared lemming in particular, the supraoptic nucleus is located more dorso-caudally and the paraventricular one-more dorsally. A greater amount of neurosecretory cells is found which from additional groups. The hypothalamo-hypophyseal and extrahypothalamic pathways are well pronounced. The postoptical nucleus is considerably developed. In the collared lemming it is almost equal to the supraoptic one in the amount of cells composing it. The ratio of the cells in the supraoptic and postoptic nuclei is suggested to be related to the level of the water-salt metabolism and the specific ecology of lemmings.     

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.     

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.     

Photoperiod influences the critical caloric intake necessary to maintain reproduction among male deer mice (Peromyscus maniculatus).

The concept of critical day length is well established among rodents; reproductive function is maintained when day lengths are greater than some specific threshold. In addition to day length cues, seasonal breeding in deer mice can also be regulated by food availability. The caloric threshold necessary to support reproduction remains unspecified for seasonally breeding rodents. The present study examined the interaction between photoperiod and food availability on reproductive function in adult male deer mice (Peromyscus maniculatus). A critical caloric intake profile was constructed in long (16L:8D) and short (8L:16D) photoperiods; groups of deer mice in both photoperiods either received food ad libitum or 90, 80, or 70% of their individual ad libitum food intake for 10 wk. At autopsy, paired testes, epididymides, and seminal vesicles were removed and weighed. Body mass, total body fat, and total body water contents were also obtained. Short, as compared to long, day lengths inhibited the reproductive systems of male deer mice. However, food consumption interacted with photoperiod to affect reproductive function. Significant reductions in reproductive organ size as well as spermatogenic activity were observed among short-day mice after a 10% reduction in ad libitum food intake. Long-day animals required a 20% reduction in caloric intake to depress reproductive function. Body mass and total body water content were generally unaffected by either photoperiod or food consumption. Total body fat content was reduced in short- as compared to long-day mice. Individual reproductive responsiveness to short days increased as food availability decreased.(ABSTRACT TRUNCATED AT 250 WORDS)     

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.     

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.     

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.     

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.     

Reproductive photoresponsiveness in Aethomys ineptus and A. namaquensis (Rodentia: Muridae) from southern Africa

Male Tete veld rats Aethomys ineptus and Namaqua rock mice A. namaquensis were independently subjected to a long photoperiod of 16L:8D and a short photoperiod of 8L:16D for 3 months in order to assess the effect of photoperiod on testicular function. Testicular parameters examined included testicular mass relative to body mass, testicular volume, seminiferous tubule diameters and changes in circulating plasma testosterone concentration. On a long day (LD) length, both species exhibited significantly higher testicular mass relative to body mass and testicular volume, and larger seminiferous tubule diameters. Circulating plasma testosterone concentrations in A. ineptus were not significantly different between the two photoperiodic treatments, but A. namaquensis showed significantly higher testosterone concentration in males on a LD length than on a short day (SD) length. This suggests that both A. ineptus and A. namaquensis are photoperiodically responsive to LDs.     

Highly Overlapping Winter Diet in Two Sympatric Lemming Species Revealed by DNA Metabarcoding

Sympatric species are expected to minimize competition by partitioning resources, especially when these are limited. Herbivores inhabiting the High Arctic in winter are a prime example of a situation where food availability is anticipated to be low, and thus reduced diet overlap is expected. We present here the first assessment of diet overlap of high arctic lemmings during winter based on DNA metabarcoding of feces. In contrast to previous analyses based on microhistology, we found that the diets of both collared (Dicrostonyx groenlandicus) and brown lemmings (Lemmus trimucronatus) on Bylot Island were dominated by Salix while mosses, which were significantly consumed only by the brown lemming, were a relatively minor food item. The most abundant plant taxon, Cassiope tetragona, which alone composes more than 50% of the available plant biomass, was not detected in feces and can thus be considered to be non-food. Most plant taxa that were identified as food items were consumed in proportion to their availability and none were clearly selected for. The resulting high diet overlap, together with a lack of habitat segregation, indicates a high potential for resource competition between the two lemming species. However, Salix is abundant in the winter habitats of lemmings on Bylot Island and the non-Salix portion of the diets differed between the two species. Also, lemming grazing impact on vegetation during winter in the study area is negligible. Hence, it seems likely that the high potential for resource competition predicted between these two species did not translate into actual competition. This illustrates that even in environments with low primary productivity food resources do not necessarily generate strong competition among herbivores.     

Temporal resolution of cold acclimation and de-acclimation in the Antarctic collembolan, Cryptopygus antarcticus

Abstract.  The Antarctic collembolan, Cryptopygus antarcticus (Willem), can switch its supercooling point (SCP) between 'winter' and 'summer' modes of cold hardiness over a matter of hours. High resolution temporal scaling of the acquisition and loss of cold hardiness is undertaken by assaying changes in the proportion of animals freezing below −15 °C in response to cooling rate, acclimation temperature, and access to food and moisture. Rapid de-acclimation to the 'summer' modal state is readily achieved after 1–6 h in response to warming and access to food; however, rapid acclimation to the 'winter' modal state is only evident in response to slow cooling and narrow ranges of temperature (0–5 °C). The rapid loss of cold tolerance at higher temperatures with access to food, in particular, emphasizes this species' opportunistic responses to resource availability in the short polar summers. Cold hardiness is apparently more readily traded off against nutrient acquisition than vice versa in this maritime Antarctic species.     

Metabolism,thermogenesis and daily rhythm of body temperature in the wood lemming,Myopus schisticolor

Wood lemmings (Myopus schisticolor) were captured during their autumnal migration in September and October. The animals were maintained at 12°C and under 12L:12D photoperiod. Basal metabolic rate and thermogenic capacity of the wood lemming were studied. Basal metabolic rate was 3.54 ml O₂·g^-1·h^-1, which is 215–238% of the expected value. The high basal metabolic rate seems to be typical of rodents living in high latitudes. The body temperature of the wood lemming was high (38.0–38.8°C), and did not fluctuate much during the 24-h recording. The high basal metabolic rate and the high body temperature are discussed with regard to behavioural adaptation to a low-quality winter diet. Thermogenic capacity, thermal insulation and non-shivering thermogenesis of the wood lemming displayed higher values than expected: 53.0 mW·g^-1, 0.53 mW·g^-1·C^-1 and 53.2 mW·g^-1, respectively. Brown adipose tissue showed typical thermogenic properties, although its respiratory property was fairly low, but mitochondrial protein content was high compared to other small mammals. The 24-h recording of body temperature and motor activity did not reveal whether the wood lemming is a nocturnal animal. Possibly, the expression of a circadian rhythm was masked by peculiar feeding behaviour. It is concluded that the wood lemming is well adapted to living in cold-temperature climates.Abbreviations BAT brown adipose tissue; bm, body mass - BMR basal metabolic rate - C conductance - Cox cytochrome-c-oxidase - HP heat production - HP_max maximum heat production - M metabolism - NA noradrenaline - NST non-shivering thermogenesis - NST_max maximum non-shivering thermogenesis - RMR resting metabolic rate - RQ respiratory quotient - T _a anibient temperature - T _b body temperature - T _lc lower critical temperature - UCP uncoupling protein - vO₂ oxygen consumption - vO_{2 max} maximum oxygen consumption