Oral vaccination of captive arctic foxes with lyophilized SAG2 rabies vaccine

Arctic foxes (Alopex lagopus) were immunized with lyophilized SAG2 oral rabies vaccine. The effectiveness of this vaccine was determined by serologic response and survival to challenge by rabies virus isolated from a red fox from Alaska (USA). No vaccine virus was found in saliva 1-72 hr after ingestion. At 2 wk after vaccination, all foxes had seroconverted, with rabies virus neutralizing antibody levels of 0.2-3.1 IU ml(-1). All vaccinated foxes survived to week 17 after challenge, and hippocampus, pons, and cerebellum were free of rabies virus as determined by direct immunofluorescence testing after death. One of four nonvaccinated foxes survived challenge and was free of rabies virus in neural tissue, and no rabies virus neutralizing antibody was detected in blood. Our results suggest that the lyophilized SAG2 oral rabies vaccine could be effective in arctic and subarctic regions, where freezing air and ground temperatures probably would not reduce its immunogenicity.     

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.     

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.     

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.     

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.     

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.     

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.     

Photoperiodic effects on post-weaning growth and food consumption in the collared lemming Dicrostonyx groenlandicus

The effects of long 'summer' (22L:2D) and short 'winter' (2L:22D) photoperiod on post-weaning growth and food consumption of the collared lemming were examined. Growth was described by Gompertz equations. After 10 weeks, lemmings maintained under short photoperiods developed white winter pelage and heavy bifid claws; body mass and estimated asymptotic mass were significantly greater than for lemmings reared under long photoperiod. Sexual dimorphism in body size was observed within treatments, males growing larger than females. There were no significant differences in the overall growth rate constant k as a result of either sex or photoperiod treatment. However, instantaneous growth rates (dW/dt) were significantly higher in 'winter' lemmings. Mass at weaning was a significant determinant of adult mass at 90 days.
Cumulative food consumption at 90 days was not significantly different between photoperiod groups, even though 'winter' lemmings gained more than double the mass of their 'summer' counterparts over the post-weaning period. Increased gut length observed for winter morphs may act as the physiological mechanism promoting greater gross energy efficiency.
The present study suggests that the overwintering strategy of the collared lemming with respect to body mass changes and energy requirements differs considerably from that of other microtines.     

Immunization of arctic foxes (Alopex lagopus) with oral rabies vaccine

Arctic foxes (Alopex lagopus) were successfully immunized against rabies using an orally-administered, liquid SAD-BHK21 live virus vaccine in a sausage bait. Immunization was determined by serologic response and by resistance to challenge with an arctic rabies virus strain. Virus was not shed in saliva following oral vaccination, indicating that arctic foxes would not infect other foxes after ingesting this vaccine. High antibody levels were present in all experimental foxes 2 wk following initial vaccination. A booster vaccination at 56 wk induced a significant serologic response within 1 wk, suggesting an anamnestic response but titers began to decline within 8 wk in most foxes. Foxes were observed for 16 mo following the challenge and exhibited no symptoms of rabies. The SAD-BHK21 rabies vaccine in a sausage bait system has a strong potential for vaccinating wild populations of arctic fox.     

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.     

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.     

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.     

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.     

Phylogeography and mitochondrial DNA (mtDNA) diversity in North American collared lemmings (Dicrostonyx groenlandicus)

Variation in the nucleotide sequence of the mitochondrial control region (250 bp) and the cytochrome b region (870 bp) was examined in collared lemmings (Dicrostonyx groenlandicus) from 19 localities in northern Alaska and the Canadian Arctic. The division of D. groenlandicus in two phylogeographical groups with limited divergence across the Mackenzie River is consistent with the separation of this species in more than one refugial area located to the northwest of the Laurentide ice sheet during the last glaciation. Populations of D.groenlandicus from formerly glaciated areas are no less variable than those in nonglaciated areas. Instead, the low intrapopulation and intraregional diversity estimates in D. groenlandicus are probably a result of regional bottleneck events due to range contractions during Holocene warming events. These results are consistent with findings previously reported on collared lemmings (D. torquatus) from the Eurasian Arctic.     

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.     

Standardization of an enzyme immunoassay for the in vitro potency assay of inactivated tissue culture rabies vaccines: determination of the rabies virus glycoprotein with polyclonal antisera

A non-competitive enzyme-linked immunoassay (ELISA) has been standardized to supplement the in vivo potency test used for the quality control of inactivated tissue culture vaccines against rabies. The essentials of the ELISA were: fixation of the virus in different dilutions of vaccine on the surface of microtitre plates; testing of the reference and up to six test vaccines on one plate; incubation with polyclonal antisera to rabies virus glycoprotein containing an excess of antibody; further incubation with a species-specific anti-IgG coupled to peroxidase; a final incubation with a substrate. The incubation periods were 1 h, 1 h and 30 min both at +37 degrees C. The relative potency determinations were made graphically or by a computer using a parallel line bioassay in which the potencies of the vaccines of unknown potency were tested against the reference preparation on a single microtitre plate. Under these conditions inactivated rabies vaccines of different types (virus strains, cell substrates, inactivation and concentration procedures) were tested for potency. Furthermore, it was possible with this in vitro method to assay adjuvanted vaccines, in process samples such as tissue culture supernatants with live or inactivated rabies virus, concentrates, and vaccines undergoing thermal stability tests. The rabies glycoprotein antigen-antibody reaction was highly specific according to the results and the glycoprotein content was measured quantitatively. The potency determined by the in vitro ELISA correlated with the in vivo NIH protection potency test. The lower limit of detection of the ELISA was 0.015 IU/ml. Quantitative antigen determination was possible with both homologous and heterologous antisera to rabies virus glycoprotein when vaccines of the same virus strain were tested. When the potencies of vaccines of different virus strain specificity were calculated, it was necessary to take into account the strain-specific antigenicity. Even so vaccines of high potency were found to give a stronger reaction with a heterologous serum than did weak vaccines with a homologous antiserum. Stability tests made on inactivated tissue culture vaccines such as vaccine from the human diploid cell strain (HDCS), from purified chicken embryo cell (PCEC) or from purified Vero cell rabies vaccine (PVRV), showed high stability of the glycoprotein antigen even after four months of storage at +37 degrees C or 24 h at +56 degrees C, provided that the vaccines were stored in a lyophilized state. The antigenicity of liquid vaccines was inactivated after a few hours at +56 degrees C. For tropical areas, therefore, only lyophilized vaccines should be considered.     

Use of recombinant vaccinia-rabies glycoprotein virus for oral vaccination of wildlife against rabies: innocuity to several non-target bait consuming species

The pathogenicity of a vaccinia recombinant virus expressing the rabies glycoprotein (VVTGgRAB) was tested in several wild animal species which could compete with the natural rabies host, the red fox (Vulpes vulpes) in consuming vaccine baits in Europe. The following species were included in this study: wild boar (Sus scrofa), Eurasian badger (Meles meles), wood mouse (Apodemus sylvaticus), yellow-necked mouse (Apodemus flavicollis), bank vole (Clethrionomys glareolus), common vole (Microtus arvalis), field vole (Microtus agrestis), water vole (Arvicola terrestris), common buzzard (Buteo buteo), kestrel (Falco tinnunculus), carrion crow (Corvus corone), magpie (Pica pica) and jay (Garrulus glandarius). During the observation period, the 107 animals given the VVTGgRAB vaccine orally did not show any clinical signs. Daily monitoring for 28 days and postmortem examination did not result in the detection of pox lesions in the oral mucosa or the skin in mammals or the unfeathered portions of birds. VVTGgRAB seems to multiply in the mammalian species tested, since rabies seroconversion was observed in all of them. Birds failed to develop demonstrable rabies virus-neutralizing antibody. A seroconversion against vaccinia virus was observed in two of four wild boars. Serological results obtained in badgers and wild boars also demonstrates the absence of direct or indirect horizontal transmission of the recombinant virus. The potential of the recombinant virus for the immunization of badgers against rabies also was investigated. Only 50% of the badgers orally administered with 1 x 10(8.3) TCID50 of this vaccine were protected against rabies.     

Proposal for changing the ministerial instructions for antirabies prophylaxis in the light of the experience of the Centro Antirabbico di Roma

Records of clinical assistance and of post-exposure antirabies prophylaxis from 4820 outpatients who attended the Antirabies Center of Rome following animal bites in 1986 were analysed. We observed a high proportion of people submitted to active immunization (44% received at least one shot of HDCV vaccine) in spite of the fact that rabies is absent from Central Italy since many decades in both wild and domestic animals. These considerations suggest the opportunity of a major revision of the official recommendations for rabies prevention, and we feel that different policies should be adopted in rabies enzootic areas (such as Northern Italy) compared to those where the risk is only potential. Immunization should be avoided after bites by rodents; passive immunization should be added to the vaccine after bites by wild animals in enzootic areas, while bites by cats and dogs, even uncaptured, will not be necessarily followed by vaccination in non enzootic areas.