Increased parental effort fails to buffer the cascading effects of warmer seas on common guillemot demographic rates.

Climate warming can reduce food resources for animal populations. In species exhibiting parental care, parental effort is a 'barometer' of changes in environmental conditions. A key issue is the extent to which variation in parental effort can buffer demographic rates against environmental change. Seabirds breed in large, dense colonies and globally are major predators of small fish that are often sensitive to ocean warming. We explored the causes and consequences of annual variation in parental effort as indicated by standardised checks of the proportions of chicks attended by both, one or neither parent, in a population of common guillemots Uria aalge over four decades during which there was marked variation in marine climate and chick diet. We predicted that, for parental effort to be an effective buffer, there would be a link between environmental conditions and parental effort, but not between parental effort and demographic rates. Environmental conditions influenced multiple aspects of the prey delivered by parents to their chicks with prey species, length and energy density all influenced by spring sea surface temperature (sSST) in the current and/or previous year. Overall, the mean annual daily energy intake of chicks declined significantly when sSST in the current year was higher. In accordance with our first prediction, we found that parental effort increased with sSST in the current and previous year. However, the increase was insufficient to maintain chick daily energy intake. In contrast to our second prediction, we found that increased parental effort had major demographic consequences such that growth rate and fledging success of chicks, and body mass and overwinter survival of breeding adults all decreased significantly. Common guillemot parents were unable to compensate effectively for temperature-mediated variation in feeding conditions through behavioural flexibility, resulting in immediate consequences for breeding population size because of lower adult survival and potentially longer-term impacts on recruitment because of lower productivity. These findings highlight that a critical issue for species' responses to future climate change will be the extent to which behavioural buffering can offer resilience to deteriorating environmental conditions.

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.

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.

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.

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.

Contrasting effects of summer and winter warming on body mass explain population dynamics in a food-limited Arctic herbivore.

The cumulative effects of climate warming on herbivore vital rates and population dynamics are hard to predict, given that the expected effects differ between seasons. In the Arctic, warmer summers enhance plant growth which should lead to heavier and more fertile individuals in the autumn. Conversely, warm spells in winter with rainfall (rain-on-snow) can cause 'icing', restricting access to forage, resulting in starvation, lower survival and fecundity. As body condition is a 'barometer' of energy demands relative to energy intake, we explored the causes and consequences of variation in body mass of wild female Svalbard reindeer (Rangifer tarandus platyrhynchus) from 1994 to 2015, a period of marked climate warming. Late winter (April) body mass explained 88% of the between-year variation in population growth rate, because it strongly influenced reproductive loss, and hence subsequent fecundity (92%), as well as survival (94%) and recruitment (93%). Autumn (October) body mass affected ovulation rates but did not affect fecundity. April body mass showed no long-term trend (coefficient of variation, CV = 8.8%) and was higher following warm autumn (October) weather, reflecting delays in winter onset, but most strongly, and negatively, related to 'rain-on-snow' events. October body mass (CV = 2.5%) increased over the study due to higher plant productivity in the increasingly warm summers. Density-dependent mass change suggested competition for resources in both winter and summer but was less pronounced in recent years, despite an increasing population size. While continued climate warming is expected to increase the carrying capacity of the high Arctic tundra, it is also likely to cause more frequent icing events. Our analyses suggest that these contrasting effects may cause larger seasonal fluctuations in body mass and vital rates. Overall our findings provide an important 'missing' mechanistic link in the current understanding of the population biology of a keystone species in a rapidly warming Arctic.

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.

Congruent responses to weather variability in high arctic herbivores.

Assessing the role of weather in the dynamics of wildlife populations is a pressing task in the face of rapid environmental change. Rodents and ruminants are abundant herbivore species in most Arctic ecosystems, many of which are experiencing particularly rapid climate change. Their different life-history characteristics, with the exception of their trophic position, suggest that they should show different responses to environmental variation. Here we show that the only mammalian herbivores on the Arctic islands of Svalbard, reindeer (Rangifer tarandus) and sibling voles (Microtus levis), exhibit strong synchrony in population parameters. This synchrony is due to rain-on-snow events that cause ground ice and demonstrates that climate impacts can be similarly integrated and expressed in species with highly contrasting life histories. The finding suggests that responses of wildlife populations to climate variability and change might be more consistent in Polar regions than elsewhere owing to the strength of the climate impact and the simplicity of the ecosystem.

Getting the timing right: antler growth phenology and sexual selection in a wild red deer population.

There has been growing interest in the determinants of the annual timing of biological phenomena, or phenology, in wild populations, but research on vertebrate taxa has primarily focused on the phenology of reproduction. We present here analyses of the phenology of the annual growth of a secondary sexual characteristic, antlers in red deer (Cervus elaphus) males. The long-term individual-based data from a wild population of red deer on the Isle of Rum, Scotland allow us to consider ecological factors influencing variation in the phenology of growth of antlers, and the implications of variation in antler growth phenology with respect to the phenotype of antler grown (antler mass) and annual breeding success. The phenology of antler growth was influenced by local environmental conditions: higher population density delayed both the start date (during spring) and the relative end date (in late summer) of antler growth, and warmer temperatures in the September and April prior to growth advanced start and end dates, respectively. Furthermore, there was variation between individuals in this phenotypic plasticity of start date, although not in that of end date of growth. The phenology of antler growth impacted on the morphology of antlers grown, with individuals who started and ended growth earliest having the heaviest antlers. The timing of antler growth phenology was associated with breeding success in the following mating season, independently of the mass of antlers grown: an earlier start of antler growth was associated with siring a higher number of the calves born the following spring. Our results suggest that the phenology of traits that are not directly correlated with offspring survival may also regularly show correlations with fitness.

More frequent extreme climate events stabilize reindeer population dynamics.

Extreme climate events often cause population crashes but are difficult to account for in population-dynamic studies. Especially in long-lived animals, density dependence and demography may induce lagged impacts of perturbations on population growth. In Arctic ungulates, extreme rain-on-snow and ice-locked pastures have led to severe population crashes, indicating that increasingly frequent rain-on-snow events could destabilize populations. Here, using empirically parameterized, stochastic population models for High-Arctic wild reindeer, we show that more frequent rain-on-snow events actually reduce extinction risk and stabilize population dynamics due to interactions with age structure and density dependence. Extreme rain-on-snow events mainly suppress vital rates of vulnerable ages at high population densities, resulting in a crash and a new population state with resilient ages and reduced population sensitivity to subsequent icy winters. Thus, observed responses to single extreme events are poor predictors of population dynamics and persistence because internal density-dependent feedbacks act as a buffer against more frequent events.

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.

Combining Slaughterhouse Surveillance Data with Cattle Tracing Scheme and Environmental Data to Quantify Environmental Risk Factors for Liver Fluke in Cattle.

Liver fluke infection causes serious disease (fasciolosis) in cattle and sheep in many regions of the world, resulting in production losses and additional economic consequences due to condemnation of the liver at slaughter. Liver fluke depends on mud snails as an intermediate host and infect livestock when ingested through grazing. Therefore, environmental factors play important roles in infection risk and climate change is likely to modify this. Here, we demonstrate how slaughterhouse data can be integrated with other data, including animal movement and climate variables to identify environmental risk factors for liver fluke in cattle in Scotland. We fitted a generalized linear mixed model to the data, with exposure-weighted random and fixed effects, an approach which takes into account the amount of time cattle spent at different locations, exposed to different levels of risk. This enabled us to identify an increased risk of liver fluke with increased animal age, rainfall, and temperature and for farms located further to the West, in excess of the risk associated with a warmer, wetter climate. This model explained 45% of the variability in liver fluke between farms, suggesting that the unexplained 55% was due to factors not included in the model, such as differences in on-farm management and presence of wet habitats. This approach demonstrates the value of statistically integrating routinely recorded slaughterhouse data with other pre-existing data, creating a powerful approach to quantify disease risks in production animals. Furthermore, this approach can be used to better quantify the impact of projected climate change on liver fluke risk for future studies.

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.

Identifying when weather influences life-history traits of grazing herbivores.

1. There is increasing evidence that density-independent weather effects influence life-history traits and hence the dynamics of populations of animals. Here, we present a novel statistical approach to estimate when such influences are strongest. The method is demonstrated by analyses investigating the timing of the influence of weather on the birth weight of sheep and deer. 2. The statistical technique allowed for the pattern of temporal correlation in the weather data enabling the effects of weather in many fine-scale time intervals to be investigated simultaneously. Thus, while previous studies have typically considered weather averaged across a single broad time interval during pregnancy, our approach enabled examination simultaneously of the relationships with weekly and fortnightly averages throughout the whole of pregnancy. 3. We detected a positive effect of temperature on the birth weight of deer, which is strongest in late pregnancy (mid-March to mid-April), and a negative effect of rainfall on the birthweight of sheep, which is strongest during mid-pregnancy (late January to early February). The possible mechanisms underlying these weather-birth weight relationships are discussed. 4. This study enhances our insight into the pattern of the timing of influence of weather on early development. The method is of much more general application and could provide valuable insights in other areas of ecology in which sequences of intercorrelated explanatory variables have been collected in space or in time.

Testing five hypotheses of sexual segregation in an arctic ungulate.

1. Sexual segregation occurs in most species of sexually dimorphic ungulates. At least five not mutually exclusive hypotheses have been formulated to explain patterns of social, habitat and spatial segregation; the indirect competition hypothesis (H1), the nutritional needs hypothesis (H2), the activity budget hypothesis (H3), the weather sensitivity hypothesis (H4), and the predation risk hypothesis (H5). 2. Each hypothesis has a unique set of predictions with respect to the occurrence of segregation, and how seasonality, density dependence and reproductive status affect sexual segregation. 3. We tested this set of predictions in order to separate the hypotheses H1-H5 for patterns of sexual segregation of the Svalbard reindeer based on 9 years data on seasonal estimates of spatial, habitat and social (i.e. grouping with their own sex) segregation in combination with resource selection functions. 4. Our results do not support that one single mechanism causes segregation. The activity budget hypothesis, the nutritional needs hypothesis and the weather sensitivity hypothesis were all partially supported, while the predation risk hypothesis was discarded for Svalbard reindeer because predators have been absent for at least 5000 years. Several mechanisms are thus interacting to explain the full-year pattern of sexual segregation and the combination of mechanisms varies among species and populations.

Constraints on plastic responses to climate variation in red deer.

Influences of climate on life history traits in natural populations are well documented. However, the implications of between-individual variation in phenotypic plasticity underlying observed trait-environment relationships are rarely considered due to the large, long-term datasets required for such analysis. Studies typically present correlations of annual trait means with climate or assume that individual phenotypic responses are constant. Here, we examine this additional level of variation and show that, in a red deer population on the Isle of Rum, Scotland, changes in climate generate changes in phenotype only amongst individuals who have experienced favourable ecological conditions. Examination of relationships between offspring birth weight and spring temperature within the lifetimes of individual females revealed that the tendency to respond to climate declined as the population density experienced early in life increased. The presence of such systematic variation in individual plasticity is rarely documented in the wild, and has important implications for our understanding of the environmental dependencies of traits under varying ecological conditions.

Resistance to abomasal nematodes and individual genetic variability in reindeer.

Resistance to parasites is believed to have a widespread influence on demographic and adaptive processes. In systems where parasites impose a fitness cost on their host, heterozygotes may be selected because they are more resistant to parasites than homozygotes. Our objective was to assess the relationships between genomewide individual heterozygosity and abomasal nematode burdens in female Svalbard reindeer (Rangifer tarandus platyrhynchus) after the effects of host age, locality, season, and year had been accounted for. Samples were obtained from 306 female reindeer that were culled and genotyped at nine microsatellite loci. Reindeer in our study populations are mainly parasitized by the gastrointestinal nematodes Ostertagia gruehneri and Marshallagia marshalli. The infection intensity of each parasite differed between subpopulations, and among host age classes, seasons and years. We found no significant relationships between abomasal worm burdens, or lumen and mucosa larvae, of either O. gruehneri or M. marshalli and individual heterozygosity (or mean d(2)) alone or in interactions with host age, locality, and year. Although we analysed one of the largest data set available to date on gastrointestinal nematodes of a wild ruminant, we used a typical data set of nine genetic neutral markers that may have had low power to detect heterozygosity-fitness correlations. We conclude that the proportion of the variance in parasite resistance explained by individual heterozygosity for neutral genetic markers is low in Svalbard reindeer and in vertebrates in general, and we suggest that the candidate-gene approach might be more fruitful for further research on gene-fitness correlations.