Disease transmission in an extreme environment: nematode parasites infect reindeer during the Arctic winter

Parasitic nematodes are found in almost all wild vertebrate populations but few studies have investigated these host-parasite relationships in the wild. For parasites with free-living stages, the external environment has a major influence on life-history traits, and development and survival is generally low at sub-zero temperatures. For reindeer that inhabit the high Arctic archipelago of Svalbard, parasite transmission is expected to occur in the summer, due to the extreme environmental conditions and the reduced food intake by the host in winter. Here we show experimentally that, contrary to most parasitic nematodes, Marshallagia marshalli of Svalbard reindeer is transmitted during the Arctic winter. Winter transmission was demonstrated by removing parasites in the autumn, using a novel delayed-release anthelmintic bolus, and estimating re-infection rates in reindeer sampled in October, February and April. Larval stages of nematodes were identified using molecular tools, whereas adult stages were identified using microscopy. The abundance of M. marshalli adult worms and L4s increased significantly from October to April, indicating that reindeer were being infected with L3s from the pasture throughout the winter. To our knowledge, this study is the first to experimentally demonstrate over-winter transmission of a gastro-intestinal nematode parasite in a wild animal. Potential mechanisms associated with this unusual transmission strategy are discussed in light of our knowledge of the life-history traits of this parasite.     

The role of parasites in the dynamics of a reindeer population

Even though theoretical models show that parasites may regulate host population densities, few empirical studies have given support to this hypothesis. We present experimental and observational evidence for a host-parasite interaction where the parasite has sufficient impact on host population dynamics for regulation to occur. During a six year study of the Svalbard reindeer and its parasitic gastrointestinal nematode Ostertagia gruehneri we found that anthelminthic treatment in April-May increased the probability of a reindeer having a calf in the next year, compared with untreated controls. However, treatment did not influence the over-winter survival of the reindeer. The annual variation in the degree to which parasites depressed fecundity was positively related to the abundance of O. gruehneri infection the previous October, which in turn was related to host density two years earlier. In addition to the treatment effect, there was a strong negative effect of winter precipitation on the probability of female reindeer having a calf. A simple matrix model was parameterized using estimates from our experimental and observational data. This model shows that the parasite-mediated effect on fecundity was sufficient to regulate reindeer densities around observed host densities.     

Rumen microbial diversity in Svalbard reindeer, with particular emphasis on methanogenic archaea

Ruminal methanogens, bacteria and ciliate protozoa of Svalbard reindeer grazing natural pastures in October (late fall) and April (late winter) were investigated using molecular-based approaches. The appetite of the Svalbard reindeer peaks in August (summer) and is at its lowest in March (winter). Microbial numbers, quantified by real-time PCR, did not change significantly between October and April, when food intakes are at similar levels, although the numbers of methanogens tended to be higher in October ( P =0.074), and ciliate numbers tended to be higher in April ( P= 0.055). Similarly, no change was detected in the bacterial and protozoal population composition by rRNA gene-based denaturing gradient gel electrophoresis analysis. Dominant methanogens were identified using a 16S rRNA gene library (97 clones) prepared from pooled PCR products from reindeer on October pasture ( n =5). Eleven of the 22 distinct operational taxonomic units (OTUs) generated exhibited a high degree of sequence similarity to methanogens affiliated with Methanobacteriales (eight OTUs), Methanomicrobiales (one OTU) and Methanosarcinales (two OTUs). The remaining 11 OTUs (53% of the clones) were associated with a cluster of uncultivated ruminal archaea. This study has provided important insights into the rumen microbiome of a high-arctic herbivorous animal living under harsh nutritional conditions, and evidence suggesting that host type affects the population size of ruminal methanogens.     

Adaptations to the Arctic: low-temperature development and cold tolerance in the free-living stages of a parasitic nematode from Svalbard

For nematodes with a direct life cycle, transmission is highly dependent on temperature-related development and survival of the free-living stages. Therefore, in the Arctic, where the winter lasts from October to May, nematode transmission is expected to be focused in the short summer season, yet there is strong evidence that as well as focussing egg output during winter months, the nematode parasite, Marshallagia marshalli, infects Svalbard reindeer during the Arctic winter when temperatures are persistently below freezing. To investigate the potential for development and survival of eggs and infective third-stage larvae in winter and therefore the possibility of for winter transmission, we ran a series of low-temperature laboratory experiments. These provide five key insights into the transmission and survival of the free-living stages of M. marshalli: (1) eggs hatched at temperatures as low as 2 °C, but not below 0 °C, (2) eggs were viable and developed after being exposed to sub-zero temperatures for up to 28 months, (3) infective-stage larvae survived for up to 80 days at 5 °C, (4) infective-stage larvae could survive rapid exposure to temperatures below ?30 °C, and (5) desiccation resistance may be important for long-term larval survival at low temperatures. Together, these results indicate that eggs deposited during the winter are highly tolerant of prevailing environmental conditions and have the potential for rapid development with the onset of spring. It is therefore likely that the parasite remains in the egg stage in the faeces during the winter of deposition, hatch and develop into the infective larval stage in the summer, remaining viable on the tundra until the reindeer host returns to the winter feeding grounds the following winter.     

Observational evidence of risk-sensitive reproductive allocation in a long-lived mammal

Organisms should adopt a risk-sensitive reproductive allocation when summer reproductive allocation competes with survival in the coming winter. This trade off is shown through autumn female body mass, which acts as an insurance against unpredictable winter environmental conditions. We tested this hypothesis on female reindeer in a population that has experienced a time period of dramatic increase in abundance. Environmental conditions during winter were fairly stable (with the exception of 1 year). We conclude that increased population abundance (perhaps in interaction with winter environmental conditions) could have represented a worsening of winter environmental conditions as both autumn offspring and spring female body mass decreased during the course of the study. Moreover, we found that the cost of reproduction was related to environmental conditions as: (1) autumn body mass was larger for barren than for lactating females, and this difference was temporally highly variable; (2) lactating females produced smaller offspring than barren ones in the following year; and (3) reproductive output (offspring size) decreased over time. We also found evidence of quality effects as lactating females had a higher reproductive success in the following year. In sum, a worsening of winter conditions lead to: (1) decreased reproductive output; (2) lowered autumn body mass for lactating females; and (3) increased body mass for barren females. Since females reduce their reproductive allocation as winter conditions becomes more severe, we conclude that reindeer have adopted a risk-sensitive reproductive allocation.     

Humoral immunity and output of first-stage larvae of Elaphostrongylus rangiferi (Nematoda, Metastrongyloidea) by infected reindeer, Rangifer tarandus tarandus

The use of an indirect immunofluorescence technique demonstrated that serum from reindeer, Rangifer tarandus tarandus, infected with Elaphostrongylus rangiferi (Nematoda, Metastrongyloidea) contained antibodies directed against antigen(s) on the cuticle of the parasites first-stage larvae (L1). Output of L1 from the male reindeer was low in the period June to August, but increased to a higher level during the rutting season (September to October). The titre of specific antibody showed an inverse pattern. In the female reindeer, larval output remained high throughout the sampling period from January to July. During this period antibody titre was low. A relationship between stress (rutting season or calving period), immunity and larval output is suggested.     

Faecal avoidance and the risk of infection by nematodes in a natural population of reindeer

We tested whether Svalbard reindeer (Rangifer tarandus platyrhynchus) minimise the risk of gastro- intestinal nematode infection by avoiding patches with a high density of faeces. This experiment was performed in preferred summer foraging habitat. The possibility that reindeer assess infection risk on the basis of faecal contamination levels across plant communities was determined by measuring the distribution of faeces in seven plant communities, and nematode developmental success in two plant communities with contrasting soil moisture content. We explored whether variation within individual reindeer in the levels of infection by gastro-intestinal nematodes was related to their diet. Reindeer avoided pastures where faecal contamination was increased, and thereby potentially reduced the risk of becoming infected by Trichostrongyle nematodes. Dung density was inversely related to soil moisture content, with high densities of faeces in dry plant communities and low densities in wet communities. However, nematode developmental success was positively related to soil moisture content, and was highest in the wetter sites. Thus, by avoiding dry areas with high dropping densities, reindeer would tend to feed in wetter areas where nematodes thrive. Therefore, dung density may be an unreliable predictor of the risk of infection. The absence of a strong relationship between an individual’s infection level and its diet might be due to the unpredictability of pasture infection level. Received: 8 July 1999 / Accepted: 20 January 2000     

Abundance and accessibility of forage for reindeer in forests of Northern Sweden: Impacts of landscape and winter climate regime

The survival of reindeer during winter, their period of greatest food stress, depends largely on the abundance and accessibility of forage in their pastures. In Northern Sweden, realized availability of forage is notably affected by snow conditions and the impacts of forestry. While these factors have been examined in isolation, their combined effect has, to the best of our knowledge to date, not been researched. In this study, vegetation surveys and analysis of snow conditions were undertaken in forest stands at various stages of recovery from clear‐cutting. The variation in abundance and growth of understory species edible by reindeer, such as lichen, was noted as forests matured. The barrier effect of ice lenses in the snow was also measured in these stands. Lichen biomass was significantly affected by a combination of stand maturity, understory vegetation height, and lichen height. Soil disturbance from the processes of felling and competition in the vegetation communities recovering from this disturbance were identified as key drivers of change in lichen biomass. Overall, clear‐cut forests had some of the greatest prevalence of ice lenses in the snow column, and forage availability at these sites was up to 61% less than in mature stands over 58 years in age. It is suggested that alternative silviculture methods are investigated for use in this reindeer herding region, as frequent clear‐cutting and consequent reduction in the average forest stand age and maturity class may be detrimental to reindeer grazing, reducing both abundance of forage, and access to it during winter.     

Development and application of a delayed-release anthelmintic intra-ruminal bolus system for experimental manipulation of nematode worm burdens

In order to quantify the impact of parasites on host population dynamics, experimental manipulations that perturb the parasite-host relationship are needed but, logistically, this is difficult for wild hosts. Here, we describe the use of a delayed-release anthelmintic delivery system that can be administered when the hosts can be captured and its activity delayed until a more appropriate period in the host-parasite cycle. Our model system is Svalbard reindeer infected with a nematode parasite, Marshallagia marshalli, which appears to accumulate during the Arctic winter. To determine the extent to which this occurs and the effect on host fitness, reindeer need to be treated with anthelmintics in late autumn but they can only be caught and handled in April. To solve this problem, we devised an intra-ruminal capsule that releases the anthelmintic from up to 6 months after being administered. The capsule was trialed in cannulated sheep and red deer to determine optimum capsule orifice size and release rates. Capsules were estimated to release placebo for 100-153 days followed by abamectin for 22-34 days. To test the efficacy of treatment in reindeer, capsules were administered in April and retrieved in October. All capsules had fully released the anthelmintic and treated reindeer had significantly lower worm burdens than controls. Thus, success of this system allows repeated treatment over several years to test the effect of winter parasitism on host fitness.     

Current state of forage resources and feeding of reindeer (<Emphasis Type="Italic">Rangifer tarandus</Emphasis>) and musk oxen (<Emphasis Type="Italic">Ovibos moschatus</Emphasis>) in the arctic tundras of Wrangel Island

The species composition and aboveground biomass of plant and lichens and the composition of reindeer and musk ox diet in the arctic tundra of Wrangel Island were studied in 2004 to 2007. The above-ground phytomass in different areas of the island varied from 1105 to 2100 kg/ha. The composition of plants consumed by reindeer and musk oxen and their proportions in the diet were determined by standard micro-histological analysis of plant remains in their feces. The results showed that, either in winter or in summer, both species obviously preferred feeding on willows (Salicaceae), which comprised almost half of their diet. Moreover, their feeding was highly selective, especially with respect to sedges and rushes (Cyperaceae + Juncaceae) and legumes (Fabaceae). Although the contributions of these plant groups to the total aboveground phytomass were very small (less than 4 and 8%), their proportions in the diet reached 27 and 24%, respectively. Mosses were not a preferred forage: their proportion in the aboveground phytomass reached 40%, but that in the diets of both species was below 10% in summer and increased to 20% only in the winter diet of reindeer. At a high abundance of lichens (up to 20% of the aboveground phytomass), neither of the animals consumed them during the study period.     

The effect of domestic sheep on forage plants of wild reindeer; a landscape scale experiment

Domestic herbivores often compete with wildlife for limited resources, and on longer time-scales, grazing may also increase or decrease coverage of important food plants to wildlife affecting the threshold density for when competition can be expected. In Norway, there are growing concerns about the effect of releasing 2.1 million domestic sheep (Ovis aries) for summer grazing into areas hosting wild populations of alpine reindeer (Rangifer tarandus). We quantified the effect of sheep grazing (0, 25 and 80 sheep/km²) on the development in coverage and abundance of plants known to be important in the diet of reindeer during summer (vascular plants) and winter (lichens) within a fully replicated, landscape scale (2.7 km²) experiment. From 2001 to 2005, the sedge, Carex bigelowii, increased while the herb Solidago virgaurea decreased in frequency at high density of sheep relative to controls (both marginally non-significant). There was no marked development in Deschampsia flexuosa, Salix herbacea or Hierarcium alpinum that could be related to sheep grazing intensity. Lichen coverage and height both decreased at high density of sheep from 2002 to 2005. Effects of low grazing intensity were closer to controls than to high grazing intensity. Our study highlights that high sheep grazing intensity induce changes to the plant community that, at the same time, can improve the summer habitat and detriment the winter habitat to reindeer. Many wild reindeer populations are fragmented and may thus be limited by either summer or winter range. The effect of sheep grazing is predicted to vary accordingly. However, currently, we have limited ability to quantify how much this explicitly means in terms of increased or reduced carrying capacity for reindeer.     

High Female Mortality Resulting in Herd Collapse in Free-Ranging Domesticated Reindeer (Rangifer tarandus tarandus) in Sweden

Reindeer herding in Sweden is a form of pastoralism practised by the indigenous Sámi population. The economy is mainly based on meat production. Herd size is generally regulated by harvest in order not to overuse grazing ranges and keep a productive herd. Nonetheless, herd growth and room for harvest is currently small in many areas. Negative herd growth and low harvest rate were observed in one of two herds in a reindeer herding community in Central Sweden. The herds (A and B) used the same ranges from April until the autumn gathering in October–December, but were separated on different ranges over winter. Analyses of capture-recapture for 723 adult female reindeer over five years (2007–2012) revealed high annual losses (7.1% and 18.4%, for herd A and B respectively). A continuing decline in the total reindeer number in herd B demonstrated an inability to maintain the herd size in spite of a very small harvest. An estimated breakpoint for when herd size cannot be kept stable confirmed that the observed female mortality rate in herd B represented a state of herd collapse. Lower calving success in herd B compared to A indicated differences in winter foraging conditions. However, we found only minor differences in animal body condition between the herds in autumn. We found no evidence that a lower autumn body mass generally increased the risk for a female of dying from one autumn to the next. We conclude that the prime driver of the on-going collapse of herd B is not high animal density or poor body condition. Accidents or disease seem unlikely as major causes of mortality. Predation, primarily by lynx and wolverine, appears to be the most plausible reason for the high female mortality and state of collapse in the studied reindeer herding community.     

Brush mouse (Peromyscus boylii) population dynamics and hantavirus infection during a warm, drought period in southern Arizona

We monitored Limestone Canyon hantavirus (LSCV) antibody prevalence, host (brush mouse, Peromyscus boylii) abundance, and environmental variables (temperature and rainfall) in brush mice captured on three trapping webs in southern Arizona for 5 yr. Although seasonal patterns were subtle, we observed large multiyear variation in population abundance and antibody prevalence. Limestone Canyon hantavirus infection in brush mouse populations varied over time with prevalence ranging from 0% to 33%. At all trapping webs, evidence of infection disappeared completely for an extended period (up to 2 yr) and eventually reappeared, suggesting that dispersal may play a role in maintaining infection in brush mouse metapopulations. Weather during the study period was drier and warmer than average and these conditions, especially during spring through fall, may have contributed to low brush mouse population density and the local extinction of LSCV during the second year of the study. Nevertheless, population growth was associated with relatively warm, dry conditions during winter periods and a cool, wet spring and summer period in the fifth year of the study. After prolonged absence, LSCV infection was consistently detected only when brush mouse population abundance reached relatively high levels during that fifth year. Comparison of our results to similar studies suggests that stochastic events resulting in the loss or survival of a few infected mice in low-density host populations may result in local extinction of virus; reestablishment of infection may occur via immigration of infected individuals from adjacent populations, but may be successful only when populations are of sufficient density to support frequent rodent-to-rodent interactions and virus transmission.     

Seasonal and ontogenetic dynamics in trophic transmission of parasites

Transmission rates from the intermediate (amphipods) to the definitive hosts (fish) were quantified for two helminth species ( Cyathocephalus truncatus , Cestoda, and Cystidicola farionis , Nematoda) both seasonally and through the ontogeny of the final hosts (arctic charr, Salvelinus alpinus , and brown trout, Salmo trutta ). Amphipods ( Gammarus lacustris ) were important prey for both fish species, especially in the autumn. Both parasite species had low infection levels in amphipods compared to high abundance in fish. The seasonal variations in transmission rate of C. truncatus procercoids from amphipods to fish were in accordance with the observed abundance in fish hosts, being highest in the autumn and lowest during late winter and early summer. During summer, however, the estimated monthly transmission rates of C. truncatus were higher than the observed infection levels in the fish, suggesting restricted establishment success and shorter development time and longevity of the cestode in fish at higher temperatures. The accumulated transmission of C. farionis over the ontogeny of arctic charr was similar to the observed age-specific infection levels, reflecting a high establishment success and longevity of this parasite in charr. In contrast, brown trout exhibited an infection level that was much lower than the estimated transmission rates, suggesting a high resistance against C. farionis in these fish. The magnitudes of the estimated transmission rates were sufficient to explain the paradoxical contrast between low infection levels in the intermediate and high in the final hosts.     

Winter Survival of Pratylenchus scribneri

Population densities of Pratylenchus scribneri in a Plainfield loamy sand soil were sampled from 1 October to 1 May for 4 years. From May to October of each year, the site was planted to Russet Burbank potato and Wis 4763 corn. Percentages of change in population densities of nematodes were computed on the basis of number of nematodes present on 1 October. The decline of P. scribneri between growing seasons was nonlinear, with most mortality occurring in the autumn before the soil froze. Winter survival, defined as the percentage of change in population densities from 1 October to 1 May the following year, ranged from 50 to 136% for nematodes in corn plots and from 15 to 86% for nematodes in potato plots. There was no difference in survival of nematodes of different life stages or among root and soil habitats. Winter survival of nematodes was density-dependent in 3 of 4 years in corn plots and in 1 of 4 years in potato plots. Although predators were present, their abundance was not correlated with the winter survival of nematodes. Cumulative and average snow cover was correlated with the survival of nematodes associated with corn but not with potato. No relationships between other climatic factors and survivorship were detected.     

Functional Anatomy of the Omasum in High Arctic Svalbard Reindeer (Rangifer tarandus platyrhynchus) and Norwegian Reindeer (Rangifer tarandus tarandus)

The structure and fill of the omasum was investigated in summer and in winter in adult female reindeer living on the polar desert and tundra of the high Arctic archipelago of Svalbard and in sub-Arctic mountain habitats in northern Norway The mean total mass of the omasum in non-lactating adult female Svalbard reindeer was 467 g (0.65 g per 100 g live body mass (BM)) in September and 477 g (1.03 g per 100 g BM) in April. By contrast, the mean mass of the omasum in non-lactating adult reindeer in northern Norway was 534 g (0.83 g per 100 g BM) in September but only 205 g (0.35 g per 100 g BM p<0.05) in late March, owing to a decrease in both tissue mass and the wet mass of the contents of the organ. The mean absorptive surface of the omasum in Svalbard reindeer was 2300 cm2 in September and 2023 cm2 in April. In Norwegian reindeer, by contrast, the absorptive surface area decreased from 2201 cm2 in September to 1181 cm2 (p<0.05) in late March. The marked seasonal decline of omasal tissue and contents in Norwegian reindeer probably results from intake of highly digestible forage plants, including lichens, in winter. Svalbard reindeer, a non-migratory sub-species, survive eating poor quality fibrous vascular plants in winter. The absence of any marked seasonal change in the mass, total absorptive surface area or filling of the omasum in Svalbard reindeer in winter despite a substantial decline in body mass presumably reflects their need to maintain maximum absorption of nutrients, including volatile fatty acids, when feeding on such poorly fermentable forage.     

Spatial heterogeneity in climate change effects decouples the long‐term dynamics of wild reindeer populations in the high Arctic

The ‘Moran effect’ predicts that dynamics of populations of a species are synchronized over similar distances as their environmental drivers. Strong population synchrony reduces species viability, but spatial heterogeneity in density dependence, the environment, or its ecological responses may decouple dynamics in space, preventing extinctions. How such heterogeneity buffers impacts of global change on large‐scale population dynamics is not well studied. Here, we show that spatially autocorrelated fluctuations in annual winter weather synchronize wild reindeer dynamics across high‐Arctic Svalbard, while, paradoxically, spatial variation in winter climate trends contribute to diverging local population trajectories. Warmer summers have improved the carrying capacity and apparently led to increased total reindeer abundance. However, fluctuations in population size seem mainly driven by negative effects of stochastic winter rain‐on‐snow (ROS) events causing icing, with strongest effects at high densities. Count data for 10 reindeer populations 8–324 km apart suggested that density‐dependent ROS effects contributed to synchrony in population dynamics, mainly through spatially autocorrelated mortality. By comparing one coastal and one ‘continental’ reindeer population over four decades, we show that locally contrasting abundance trends can arise from spatial differences in climate change and responses to weather. The coastal population experienced a larger increase in ROS, and a stronger density‐dependent ROS effect on population growth rates, than the continental population. In contrast, the latter experienced stronger summer warming and showed the strongest positive response to summer temperatures. Accordingly, contrasting net effects of a recent climate regime shift—with increased ROS and harsher winters, yet higher summer temperatures and improved carrying capacity—led to negative and positive abundance trends in the coastal and continental population respectively. Thus, synchronized population fluctuations by climatic drivers can be buffered by spatial heterogeneity in the same drivers, as well as in the ecological responses, averaging out climate change effects at larger spatial scales.     

Winter habitat–space use in a large arctic herbivore facing contrasting forage abundance

We analysed how changes in resource levels influence foraging trade-offs in late winter by wild Svalbard reindeer. Forage plants, and particularly lichens, were less abundant at the overgrazed Brøggerhalvøya compared with the neighbouring Sarsøyra. Strong interactions occurred between habitat selection, home range size, and feeding crater selection. At Brøggerhalvøya, radiocollared females generally selected productive habitat (high summer NDVI; Normalised Difference Vegetation Index). “Immigrants” at Sarsøyra (dispersed from Brøggerhalvøya in early winter) had similar habitat preferences, probably due to past experience. In contrast, “residents” at Sarsøyra were more influenced by abiotic conditions, using habitat with low NDVI, but selecting for high-quality forage (lichens) when cratering. This suggests more quality-based selection at the expense of quantity when forage abundance increases. Habitat–space use relationships also differed between the animal categories, as home range size decreased with availability of preferred habitat. Thus, changes in forage abundance can strongly influence winter habitat–space use interactions in predator-free systems.     

Overwinter body condition,mortality and parasite infection in two size classes of 0+ year juvenile European bitterling Rhodeus amarus

Body condition and parasite abundance were examined in two size classes of European bitterling Rhodeus amarus during the first overwintering period in two seasons (2007–2008 and 2009–2010). Body condition of large fish did not change during winter, and increased significantly in March. From November to February, small fish showed a decreasing trend in condition. Despite a significant increase in March condition of small fish only reached the same level as before winter. Total parasite abundance increased significantly in winter in both fish size classes, reflecting a seasonal increase in monogenean infection. Large fish were parasitized significantly more than small fish during winter, but only in small fish was a negative correlation between parasite infection and condition found and a significant decrease in parasite abundance recorded after wintering, indicating mortality of heavily infected individuals with low condition during the winter. A trend for higher overwinter mortality in small fish was found under semi‐experimental conditions. The decrease in condition during the winter period in small fish may reflect faster energy depletion generally expected in smaller individuals. The results indicate that parasite infection may contribute to the overwinter mortality of 0+ year R. amarus, with a stronger effect in smaller individuals.     

Body protein stores and isotopic indicators of N balance in female reindeer (Rangifer tarandus) during winter

We studied bred and unbred female reindeer (Rangifer tarandus tarandus) during 12 wk of winter when ambient temperatures were low and nitrogen (N) demand for fetal growth is highest in pregnant females. Animals were fed a complete pelleted diet ad lib. that contained 2.54% N in dry matter that was 80% +/- 2% (X +/- SD) digestible. Female reindeer lost 64% +/- 14% of body fat but gained 34% +/- 11% of lean mass from 10 wk prepartum to parturition. These changes were equivalent to average balances of -14.14 +/- 2.35 MJ d(-1) and 10 +/- 3 g N d(-1). Blood cells, serum, and urine declined in (15)N/(14)N in late winter as body protein was gained from the diet. Blood cells of newborn calves were more enriched in (15)N and (13)C than that of their mothers, indicating the deposition of fetal protein from maternal stores. To quantify pathways of N flow in reindeer, N balance was measured by confining animals to cages for 10 d at 4 wk from parturition. N balance was inversely related to (15)N/(14)N in urea-N but not related to (15)N/(14)N of blood cells, creatinine, and feces. The proportion of urea-N derived from body protein increased above 0.46 as N balance fell below -200 mg N kg(-0.75) d(-1). Proportions of urea-N from body protein were -0.01 +/- 0.21 in pregnant females before and after caging and were consistent with average body protein gain in winter. Storage of protein allows reindeer and caribou to tolerate diets that are low in N without impairing fetal development.