Gut microbiome biogeography in reindeer supersedes millennia of ecological and evolutionary separation.

Ruminants are dependent on their gut microbiomes for nutrient extraction from plant diets. However, knowledge about the composition, diversity, function, and spatial structure of gut microbiomes, especially in wild ruminants, is limited, largely because analysis has been restricted to faeces or the rumen. In two geographically separated reindeer subspecies, 16S rRNA gene amplicon sequencing revealed strong spatial structuring, and pronounced differences in microbial diversity of at least 33 phyla across the stomach, small intestine, and large intestine (including faeces). The main structural feature was the Bacteroidota to Firmicutes ratio, which declined from the stomach to the large intestine, likely reflecting functional adaptation. Metagenome shotgun sequencing also revealed highly significant structuring in the relative occurrence of carbohydrate-active enzymes (CAZymes). CAZymes were enriched in the rumen relative to the small and large intestines. Interestingly, taxonomic diversity was highest in the large intestine, suggesting an important and understudied role for this organ. Despite the two study populations being separated by an ocean and six millennia of evolutionary history, gut microbiome structuring was remarkably consistent. Our study suggests a strong selection for gut microbiome biogeography along the gastrointestinal tract in reindeer subspecies.

Contrasting genomic consequences of anthropogenic reintroduction and natural recolonization in high-arctic wild reindeer.

Anthropogenic reintroduction can supplement natural recolonization in reestablishing a species' distribution and abundance. However, both reintroductions and recolonizations can give rise to founder effects that reduce genetic diversity and increase inbreeding, potentially causing the accumulation of genetic load and reduced fitness. Most current populations of the endemic high-arctic Svalbard reindeer (Rangifer tarandus platyrhynchus) originate from recent reintroductions or recolonizations following regional extirpations due to past overharvesting. We investigated and compared the genomic consequences of these two paths to reestablishment using whole-genome shotgun sequencing of 100 Svalbard reindeer across their range. We found little admixture between reintroduced and natural populations. Two reintroduced populations, each founded by 12 individuals around four decades (i.e. 8 reindeer generations) ago, formed two distinct genetic clusters. Compared to the source population, these populations showed only small decreases in genome-wide heterozygosity and increases in inbreeding and lengths of runs of homozygosity. In contrast, the two naturally recolonized populations without admixture possessed much lower heterozygosity, higher inbreeding and longer runs of homozygosity, possibly caused by serial population founder effects and/or fewer or more genetically related founders than in the reintroduction events. Naturally recolonized populations can thus be more vulnerable to the accumulation of genetic load than reintroduced populations. This suggests that in some organisms even small-scale reintroduction programs based on genetically diverse source populations can be more effective than natural recolonization in establishing genetically diverse populations. These findings warrant particular attention in the conservation and management of populations and species threatened by habitat fragmentation and loss.

A Summer Heat Wave Reduced Activity, Heart Rate, and Autumn Body Mass in a Cold-Adapted Ungulate.

AbstractHeat waves are becoming more frequent across the globe and may impose severe thermoregulatory challenges for endotherms. Heat stress can induce both behavioral and physiological responses, which may result in energy deficits with potential fitness consequences. We studied the responses of reindeer (Rangifer tarandus tarandus), a cold-adapted ungulate, to a record-breaking heat wave in northern Finland. Activity, heart rate, subcutaneous body temperature, and body mass data were collected for 14 adult females. The post-heat wave autumn body masses were then analyzed against longitudinal body mass records for the herd from 1990 to 2021. With increasing air temperature during the day, reindeer became less active and had reduced heart rate and increased body temperature, reflecting both behavioral and physiological responses to heat stress. Although they increased activity in the late afternoon, they failed to compensate for lost foraging time on the hottest days (daily mean temperature ≥20°C), and total time active was reduced by 9%. After the heat wave, the mean September body mass of herd females (69.7±6.6 kg, n=52) was on average 16.4% ± 4.8% lower than predicted (83.4±6.0 kg). Among focal females, individuals with the lowest levels of activity during the heat wave had the greatest mass loss during summer. We show how heat waves impose a thermoregulatory challenge on endotherms, resulting in mass loss, potentially as a result of the loss of foraging time. While it is well known that environmental conditions affect large herbivore fitness indirectly through decreased forage quality and limited water supply, direct effects of heat may be increasingly common in a warming climate.

Stress responses to repeated captures in a wild ungulate.

While capture-mark-recapture studies provide essential individual-level data in ecology, repeated captures and handling may impact animal welfare and cause scientific bias. Evaluating the consequences of invasive methodologies should be an integral part of any study involving capture of live animals. We investigated short- and long-term stress responses to repeated captures within a winter on the physiology, behaviour, and reproductive success of female Svalbard reindeer (Rangifer tarandus platyrhynchus). Short-term responses were evaluated using serum concentrations of glucocorticoids and catecholamines during handling, and post-release recovery times in heart rate and activity levels. Repeated captures were associated with an increase in measured catecholamines and glucocorticoids, except cortisone, and delayed recovery in heart rate but not activity. Four months later, in summer, individuals captured repeatedly in winter exhibited a small increase in behavioural response to human disturbance and had a lower probability of being observed with a calf, compared to animals not captured, or captured only once. Our findings imply that single annual capture events have no significant negative consequences for Svalbard reindeer, but repeated captures within a season may impact offspring survival in the same year. Such unanticipated side effects highlight the importance of addressing multiple indicators of animal responses to repeated captures.

Harvesting can stabilise population fluctuations and buffer the impacts of extreme climatic events.

Harvesting can magnify the destabilising effects of environmental perturbations on population dynamics and, thereby, increase extinction risk. However, population-dynamic theory predicts that impacts of harvesting depend on the type and strength of density-dependent regulation. Here, we used logistic population growth models and an empirical reindeer case study to show that low to moderate harvesting can actually buffer populations against environmental perturbations. This occurs because of density-dependent environmental stochasticity, where negative environmental impacts on vital rates are amplified at high population density due to intra-specific resource competition. Simulations from our population models show that even low levels of harvesting may prevent overabundance, thereby dampening population fluctuations and reducing the risk of population collapse and quasi-extinction following environmental perturbations. Thus, depending on the species' life history and the strength of density-dependent environmental drivers, low to moderate harvesting can improve population resistance to increased climate variability and extreme weather expected under global warming.

Context-dependent fitness costs of reproduction despite stable body mass costs in an Arctic herbivore.

The cost of reproduction on demographic rates is often assumed to operate through changing body condition. Several studies have found that reproduction depresses body mass more if the current conditions are severe, such as high population densities or adverse weather, than under benign environmental conditions. However, few studies have investigated the association between the fitness components and body mass costs of reproduction. Using 25 years of individual-based capture-recapture data from Svalbard reindeer Rangifer tarandus platyrhynchus, we built a novel Bayesian state-space model that jointly estimated interannual change in mass, annual reproductive success and survival, while accounting for incomplete observations. The model allowed us to partition the differential effects of intrinsic and extrinsic factors on both non-reproductive mass change and the body mass cost of reproduction, and to quantify their consequences on demographic rates. Contrary to our expectation, the body mass cost of reproduction (mean = -5.8 kg) varied little between years (CV = 0.08), whereas the between-year variation in body mass changes, that were independent of the previous year's reproductive state, varied substantially (CV = 0.4) in relation to autumn temperature and the amount of rain-on-snow in winter. This body mass loss led to a cost of reproduction on the next reproduction, which was amplified by the same environmental covariates, from a 10% reduction in reproductive success in benign years, to a 50% reduction in harsh years. The reproductive mass loss also resulted in a small reduction in survival. Our results show how demographic costs of reproduction, driven by interannual fluctuations in individual body condition, result from the balance between body mass costs of reproduction and body mass changes that are independent of previous reproductive state. We illustrate how a strong context-dependent fitness cost of reproduction can occur, despite a relatively fixed body mass cost of reproduction. This suggests that female reindeer display a very conservative energy allocation strategy, either aborting their reproductive attempt at an early stage or weaning at a relatively constant cost. Such a strategy might be common in species living in a highly stochastic and food limited environment.

Determinants of heart rate in Svalbard reindeer reveal mechanisms of seasonal energy management.

Seasonal energetic challenges may constrain an animal's ability to respond to changing individual and environmental conditions. Here, we investigated variation in heart rate, a well-established proxy for metabolic rate, in Svalbard reindeer (Rangifer tarandus platyrhynchus), a species with strong seasonal changes in foraging and metabolic activity. In 19 adult females, we recorded heart rate, subcutaneous temperature and activity using biologgers. Mean heart rate more than doubled from winter to summer. Typical drivers of energy expenditure, such as reproduction and activity, explained a relatively limited amount of variation (2-6% in winter and 16-24% in summer) compared to seasonality, which explained 75% of annual variation in heart rate. The relationship between heart rate and subcutaneous temperature depended on individual state via body mass, age and reproductive status, and the results suggested that peripheral heterothermy is an important pathway of energy management in both winter and summer. While the seasonal plasticity in energetics makes Svalbard reindeer well-adapted to their highly seasonal environment, intraseasonal constraints on modulation of their heart rate may limit their ability to respond to severe environmental change. This study emphasizes the importance of encompassing individual state and seasonal context when studying energetics in free-living animals. This article is part of the theme issue 'Measuring physiology in free-living animals (Part II)'.

The neglected season: Warmer autumns counteract harsher winters and promote population growth in Arctic reindeer.

Arctic ungulates are experiencing the most rapid climate warming on Earth. While concerns have been raised that more frequent icing events may cause die-offs, and earlier springs may generate a trophic mismatch in phenology, the effects of warming autumns have been largely neglected. We used 25 years of individual-based data from a growing population of wild Svalbard reindeer, to test how warmer autumns enhance population growth. Delayed plant senescence had no effect, but a six-week delay in snow-onset (the observed data range) was estimated to increase late winter body mass by 10%. Because average late winter body mass explains 90% of the variation in population growth rates, such a delay in winter-onset would enable a population growth of r = 0.20, sufficient to counteract all but the most extreme icing events. This study provides novel mechanistic insights into the consequences of climate change for Arctic herbivores, highlighting the positive impact of warming autumns on population viability, offsetting the impacts of harsher winters. Thus, the future for Arctic herbivores facing climate change may be brighter than the prevailing view.

Sea ice loss increases genetic isolation in a high Arctic ungulate metapopulation.

Sea ice loss may have dramatic consequences for population connectivity, extinction-colonization dynamics, and even the persistence of Arctic species subject to climate change. This is of particular concern in face of additional anthropogenic stressors, such as overexploitation. In this study, we assess the population-genetic implications of diminishing sea ice cover in the endemic, high Arctic Svalbard reindeer (Rangifer tarandus platyrhynchus) by analyzing the interactive effects of landscape barriers and reintroductions (following harvest-induced extirpations) on their metapopulation genetic structure. We genotyped 411 wild reindeer from 25 sampling sites throughout the entire subspecies' range at 19 microsatellite loci. Bayesian clustering analysis showed a genetic structure composed of eight populations, of which two were admixed. Overall population genetic differentiation was high (mean FST  = 0.21). Genetic diversity was low (allelic richness [AR] = 2.07-2.58; observed heterozygosity = 0.23-0.43) and declined toward the outer distribution range, where populations showed significant levels of inbreeding. Coalescent estimates of effective population sizes and migration rates revealed strong evolutionary source-sink dynamics with the central population as the main source. The population genetic structure was best explained by a landscape genetics model combining strong isolation by glaciers and open water, and high connectivity by dispersal across winter sea ice. However, the observed patterns of natural isolation were strongly modified by the signature of past harvest-induced extirpations, subsequent reintroductions, and recent lack of sea ice. These results suggest that past and current anthropogenic drivers of metapopulation dynamics may have interactive effects on large-scale ecological and evolutionary processes. Continued loss of sea ice as a dispersal corridor within and between island systems is expected to increase the genetic isolation of populations, and thus threaten the evolutionary potential and persistence of Arctic wildlife.

Silver spoon effects are constrained under extreme adult environmental conditions.

Early-life environmental conditions may generate cohort differences in individual fitness, subsequently affecting population growth rates. Three, nonmutually exclusive hypotheses predict the nature of these fitness differences: (1) silver spoon effects, where individuals born in good conditions perform better across the range of adult environments; (2) the "environmental saturation" hypothesis, where fitness differences only occur in intermediate adult environmental conditions; and (3) the "environmental matching" or "predictive adaptive response" (PAR) hypothesis, where fitness is highest when adult environmental conditions match those experienced in early life. We quantified the context-dependent effect of early-life environment on subsequent reproductive success, survival, and population growth rate (λ) of Svalbard reindeer, and explored how well it was explained by the three hypotheses. We found that good early-life conditions increased reproductive success compared to poor early-life conditions, but only when experiencing intermediate adult environmental conditions. This is the first example of what appears to be both "beneficial" and "detrimental environmental saturation" in a natural system. Despite weak early-life effects on survival, cohorts experiencing good early-life conditions contributed to higher population growth rates, when simulating realistic variation in adult environmental conditions. Our results show how the combination of a highly variable environment and biological constraints on fitness components can suppress silver spoon effects at both extremes of the adult environmental gradient.

Future suitability of habitat in a migratory ungulate under climate change.

With climate change, the effect of global warming on snow cover is expected to cause range expansion and enhance habitat suitability for species at their northern distribution limits. However, how this depends on landscape topography and sex in size-dimorphic species remains uncertain, and is further complicated for migratory animals following climate-driven seasonal resource fluctuations across vast landscapes. Using 11 years of data from a partially migratory ungulate at their northern distribution ranges, the red deer ( Cervus elaphus), we predicted sex-specific summer and winter habitat suitability in diverse landscapes under medium and severe global warming. We found large increases in future winter habitat suitability, resulting in expansion of winter ranges as currently unsuitable habitat became suitable. Even moderate warming decreased snow cover substantially, with no suitability difference between warming scenarios. Winter ranges will hence not expand linearly with warming, even for species at their northern distribution limits. Although less pronounced than in winter, summer ranges also expanded and more so under severe warming. Summer habitat suitability was positively correlated with landscape topography and ranges expanded more for females than males. Our study highlights the complexity of predicting future habitat suitability for conservation and management of size-dimorphic, migratory species under global warming.

Antler growth as a cost of reproduction in female reindeer.

The costs of reproduction are important in shaping individual life histories, and hence population dynamics, but the mechanistic pathways of such costs are often unknown. Female reindeer have evolved antlers possibly due to interference competition on winter-feeding grounds. Here, we investigate if variation in antler size explains part of the cost of reproduction in late winter mass of female reindeer. We captured 440 individual Svalbard reindeer a total of 1426 times over 16 years and measured antler size and body mass in late winter, while presence of a 'calf-at-heel' was observed in summer. We found that reproductive females grew smaller antlers and weighed 4.3 kg less than non-reproductive females. Path analyses revealed that 14% of this cost of reproduction in body mass was caused by the reduced antler size. Our study is therefore consistent with the hypothesis that antlers in female Rangifer have evolved due to interference competition and provides evidence for antler growth as a cost of reproduction in females. Antler growth was constrained more by life history events than by variation in the environment, which contrasts markedly with studies on male antlers and horns, and hence increases our understanding of constraints on ornamentation and life history trade-offs.

Biased estimation of trends in cohort effects: the problems with age-period-cohort models in ecology.

Environmental variation can generate life-long similarities among individuals born in the same breeding event, so-called cohort effects. Studies of cohort effects have to account for the potentially confounding effects of current conditions (observation year) and age of individuals. However, estimation of such models is hampered by inherent collinearity, as age is the difference between observation year (period) and cohort year. The difficulties of separating linear trends in any of the three variables in Age-Period-Cohort (APC) models are the subject of ongoing debate in social sciences and medicine but have remained unnoticed in ecology. After reviewing the use of APC models, we investigate the consequences of model specification on the estimation of cohort effects, using both simulated data and empirical data from a long-term individual-based study of reindeer in Svalbard. We demonstrate that APC models are highly sensitive to the model's treatment of age, period and cohort, which may generate spurious temporal trends in cohort effects. Avoiding grouping ages and using environmental covariates believed to be drivers of temporal variation reduces the APC identification problem. Nonetheless, ecologists should use caution, given that the specification issues in APC models may have substantial impacts on estimated effect sizes and therefore conclusions.

Circadian rhythmicity persists through the Polar night and midnight sun in Svalbard reindeer.

Studies of locomotor activity in Svalbard reindeer reported the temporary absence of diel rhythms under Arctic photic conditions. However, using Lomb-Scargle periodogram analyses with high statistical power we found diel or circadian rhythmicity throughout the entire year in measures of behaviour, temperature in the rumen and heart rate in free-living Svalbard reindeer. Significant diel rhythmicity was only lacking during some of the 15-day intervals analysed in the less frequently measured heart rate. During Polar Night these rhythms were free-running and attenuated. During continual daylight in summer, rhythms where entrained to 24 hours corresponding with the daily variation in the intensity of solar radiation, but attenuated when continuous daylight coincided with the period of growing forage. Diel rhythmicity was reduced during this short period of peak foraging activity, which coincided with peak heart rate and temperature in the rumen, most likely to facilitate fattening when food is abundant. For the rest of the year, heart rate and temperature showed the most pronounced and long-lasting suppression ever found in ungulates. The profound seasonal changes in foraging, metabolic activity, and power of diel and circadian rhythmicity of Svalbard reindeer can be viewed as adaptations to the extreme living conditions in the High Arctic.

The influence of weather conditions during gestation on life histories in a wild Arctic ungulate.

The internal predictive adaptive response (internal PAR) hypothesis predicts that individuals born in poor conditions should start to reproduce earlier if they are likely to have reduced performance in later life. However, whether this is the case remains unexplored in wild populations. Here, we use longitudinal data from a long-term study of Svalbard reindeer to examine age-related changes in adult female life-history responses to environmental conditions experienced in utero as indexed by rain-on-snow (ROSutero). We show that females experiencing high ROSutero had reduced reproductive success only from 7 years of age, independent of early reproduction. These individuals were able to maintain the same annual reproductive success between 2 and 6 years as phenotypically superior conspecifics that experienced low ROSutero Young females born after high ROSutero engage in reproductive events at lower body mass (about 2.5 kg less) than those born after low ROSutero The mean fitness of females that experienced poor environmental conditions in early life was comparable with that of females exposed to good environmental conditions in early life. These results are consistent with the idea of internal PAR and suggest that the life-history responses to early-life conditions can buffer the delayed effects of weather on population dynamics.

The influence of red deer space use on the distribution of Ixodes ricinus ticks in the landscape.

BACKGROUND: Many wingless ectoparasites have a limited capacity for active movement and are therefore primarily dependent on hitchhiking on their hosts for transportation. The distribution of the tick Ixodes ricinus is expected to depend mainly on transportation by hosts and tick subsequent survival in areas where they drop off. In Europe, the most important hosts of adult female I. ricinus are cervids. The extensive space use of large hosts provides a much larger dispersal potential for I. ricinus than that of smaller mammalian hosts. We aim to determine the contribution of red deer (Cervus elaphus) space use on the spatial distribution of I. ricinus, after accounting for landscape factors. METHODS: We analysed the spatial distribution of I. ricinus with generalised mixed effects models (GLMMs) based on data from extensive field surveys of questing density in two coastal regions in Norway, from which home range data from 73 red deer with GPS collars were available. Red deer home ranges were derived using the kernel method to identify areas most frequently used by deer. We first fitted a baseline model with tick questing densities relative to landscape features that are likely to affect local climate conditions and hence, survival. We then added deer space use variables to the baseline model with only landscape variables to test whether areas more frequently used by red deer had higher questing tick densities. RESULTS: Questing I. ricinus density was predicted by several landscape features, such as elevation, distance to the fjord and topographic slope. In addition, we found that areas more heavily used within the red deer home ranges, correlated with higher questing tick densities. Increased effects of deer space use were additive to the landscape model, suggesting that correlations were more than just shared landscape preferences between deer and ticks. CONCLUSIONS: Our results imply that the distribution of I. ricinus is controlled by a complex set of factors that include both local conditions related to landscape properties that affect survival and how the large host population redistributes ticks. In particular, we have provided evidence that the local distribution of large hosts, with their extensive space use, redistributes ticks at the local scale.

Leave before it's too late: anthropogenic and environmental triggers of autumn migration in a hunted ungulate population.

Autumn has to a large extent been neglected in the climate effect literature, yet autumn events, e.g., plant senescence and animal migration, affect fitness of animals differently than spring events. Understanding how variables including plant phenology influence timing of autumn migrations is important to gain a comprehensive understanding of the full annual cycle of migratory species. Here we use 13 yr of data from 60 male and 168 female red deer (Cervus elaphus) to identify triggers of autumn migration. We relate the timing of autumn migration to environmental variables like snow fall, temperature, and plant phenology (NDVI), and to onset of hunting, sex, and migration distance. Severe weather has been suggested as the main trigger of autumn migration, but we found that the majority of the individuals had left the summer range well before snow fall (80.3%) and frost (70.5%), and also before the peak deterioration in forage quality (71.9%). Declining temperatures were associated with a higher daily migration potential. Onset of hunting showed the largest effect on migration potential, with a marked increase during the first days of hunting. Individuals still present in the summer range when snow fall, frost, or peak forage deterioration occurred showed a significantly higher migration potential around these events. Males were less responsive to environmental cues, suggesting rutting activity, starting earlier in males, initiate movement prior to such conditions. Also, individuals with longer migration distances had a higher migration potential late in the season than individuals with shorter migration distances. Our study shows that factors beyond weather and plant phenology, such as onset of hunting, may be important triggers of autumn migration. Severe weather and forage deterioration were important triggers for the individuals experiencing this, which suggests a hierarchical response to environmental cues. The trade-off between staying longer in the summer range and increased energy expenditures if surprised by severe weather is asymmetric, and leaving well in advance can be seen as a risk-averse tactic.

Demographic buffering of life histories? Implications of the choice of measurement scale.

Life-history theory predicts that the vital rates that influence population growth the most should be buffered against environmental fluctuations due to selection for reduced variation. However, it remains unclear whether populations actually are influenced by such "demographic buffering," because variation in vital rates can be compared on different measurement scales, and there has been little attempt to investigate whether the choice of scale influences the chance of detecting demographic buffering. We compared two statistical approaches to examine whether demographic buffering has influenced vital rates in wild Svalbard reindeer (Rangifer tarandus platyrhynchus). To account for statistical variance constraints on vital rates limited between 0 and 1 in analyses of demographic buffering, one approach is to scale observed variation by the maximum possible variation on the arithmetic scale. When applying this approach, the results suggested that demographic buffering was occurring. However, when we applied an alternative approach that identified statistical variance constraints on the logit scale, there was no evidence for demographic buffering. Thus, the choice of measurement scale must be carefully considered before one can fully understand whether demographic buffering influences life histories. Defining the appropriate scale may require an understanding of the mechanisms through which demographic buffering may have evolved.

Leave before it's too late: anthropogenic and environmental triggers of autumn migration in a hunted ungulate population.

Autumn has to a large extent been neglected in the climate effect literature, yet autumn events, e.g., plant senescence and animal migration, affect fitness of animals differently than spring events. Understanding how variables including plant phenology influence timing of autumn migrations is important to gain a comprehensive understanding of the full annual cycle of migratory species. Here we use 13 yr of data from 60 male and 168 female red deer (Cervus elaphus) to identify triggers of autumn migration. We relate the timing of autumn migration to environmental variables like snow fall, temperature, and plant phenology (NDVI), and to onset of hunting, sex, and migration distance. Severe weather has been suggested as the main trigger of autumn migration, but we found that the majority of the individuals had left the summer range well before snow fall (80.3%) and frost (70.5%), and also before the peak deterioration in forage quality (71.9%). Declining temperatures were associated with a higher daily migration potential. Onset of hunting showed the largest effect on migration potential, with a marked increase during the first days of hunting. Individuals still present in the summer range when snow fall, frost, or peak forage deterioration occurred showed a significantly higher migration potential around these events. Males were less responsive to environmental cues, suggesting rutting activity, starting earlier in males, initiate movement prior to such conditions. Also, individuals with longer migration distances had a higher migration potential late in the season than individuals with shorter migration distances. Our study shows that factors beyond weather and plant phenology, such as onset of hunting, may be important triggers of autumn migration. Severe weather and forage deterioration were important triggers for the individuals experiencing this, which suggests a hierarchical response to environmental cues. The trade-off between staying longer in the summer range and increased energy expenditures if surprised by severe weather is asymmetric, and leaving well in advance can be seen as a risk-averse tactic.