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.

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.

Icing events trigger range displacement in a high-arctic ungulate.

Despite numerous studies of how climate change may affect life history of mammals, few have documented the direct impact of climate on behavior. The Arctic is currently warming, and rain-on-snow and thaw-freeze events leading to ice formation on the ground may increase both in frequency and spatial extent. This is in turn expected to be critical for the winter survival of arctic herbivores. Svalbard reindeer (Rangifer tarandus plathyrynchus) have small home ranges and may therefore be vulnerable to local "locked pasture" events (ice layers limit access to plant forage) due to ground-ice formation. When pastures are "locked," Svalbard reindeer are faced with the decision of staying and live off a diminishing fat store, or trying to escape beyond the unknown spatial borders of the ice. We demonstrate that Svalbard reindeer do the latter, as icing events cause an immediate increase in range displacement between 5-day observations. Population-level responses of previous icing events may therefore not accurately predict future responses if the spatial extent of icing increases. The impact of single events may be more severe if it exceeds the maximum movement distances, so that the spatial displacement strategy reported here no longer buffers climate effects.

Temporal scales, trade-offs, and functional responses in red deer habitat selection.

Animals selecting habitats often have to consider many factors, e.g., food and cover for safety. However, each habitat type often lacks an adequate mixture of these factors. Analyses of habitat selection using resource selection functions (RSFs) for animal radiotelemetry data typically ignore trade-offs, and the fact that these may change during an animal's daily foraging and resting rhythm on a short-term basis. This may lead to changes in the relative use of habitat types if availability differs among individual home ranges, called functional responses in habitat selection. Here, we identify such functional responses and their underlying behavioral mechanisms by estimating RSFs through mixed-effects logistic regression of telemetry data on 62 female red deer (Cervus elaphus) in Norway. Habitat selection changed with time of day and activity, suggesting a trade-off in habitat selection related to forage quantity or quality vs. shelter. Red deer frequently used pastures offering abundant forage and little canopy cover during nighttime when actively foraging, while spending much of their time in forested habitats with less forage but more cover during daytime when they are more often inactive. Selection for pastures was higher when availability was low and decreased with increasing availability. Moreover, we show for the first time that in the real world with forest habitats also containing some forage, there was both increasing selection of pastures (i.e., not proportional use) and reduced time spent in pastures (i.e., not constant time use) with lowered availability of pastures within the home range. Our study demonstrates that landscape-level habitat composition modifies the trade-off between food and cover for large herbivorous mammals. Consequently, landscapes are likely to differ in their vulnerability to crop damage and threat to biodiversity from grazing.

Negative density-dependent emigration of males in an increasing red deer population.

In species with polygynous mating systems, females are regarded as food-limited, while males are limited by access to mates. When local density increases, forage availability declines, while mate access for males may increase due to an increasingly female-biased sex ratio. Density dependence in emigration rates may consequently differ between sexes. Here, we investigate emigration using mark-recovery data from 468 young red deer Cervus elaphus marked in Snillfjord, Norway over a 20-year period when the population size has increased sixfold. We demonstrate a strong negative density-dependent emigration rate in males, while female emigration rates were lower and independent of density. Emigrating males leaving the natal range settled in areas with lower density than expected by chance. Dispersing males moved 42 per cent longer at high density in 1997 (37 km) than at low density in 1977 (26 km), possibly caused by increasing saturation of deer in areas surrounding the marking sites. Our study highlights that pattern of density dependence in dispersal rates may differ markedly between sexes in highly polygynous species. Contrasting patterns reported in small-scale studies are suggestive that spatial scale of density variation may affect the pattern of temporal density dependence in emigration rates and distances.

Maturation trends in red deer females over 39 years in harvested populations.

1. There is increasing awareness that heavy harvesting can lead to rapid evolution towards earlier sexual maturation. With increased harvest pressure, individuals that begin reproduction at light weights have a greater chance of reproducing at least once compared with individuals that begin reproduction at heavier weights and hence later in life. Although well documented in fish, this has not been empirically tested for harvested populations of mammals in terrestrial ecosystems differing in many environmental aspects. 2. Using data from 3856 female red deer (Cervus elaphus L.) from three harvested populations, we tested whether red deer maturity changed from 1967 to 2006. In these populations, density has increased markedly over the time period reducing body mass of deer, which has decreased the proportion of females maturing as yearlings. We therefore assessed trends in maturation as yearlings after controlling for body mass. Long-lived iteroparous ungulate females are expected to have a prudent life history not risking their future survival and reproduction under harsh conditions (e.g. at high density). An alternative to the harvest-induced evolution hypothesis is that maturation is driven mainly by phenotypic responses to increased density, and we predicted later maturation even after controlling for the reduction in body mass. 3. There was a marked trend towards later age at maturation in one out of three populations (after controlling for the effect of reduced body mass due to increased density), while there was no marked trend in the two other populations. The harvesting-induced evolution hypothesis was therefore not supported. However, although the decline was predicted from the prudent life-history tactic hypothesis, the estimate for the density effect was positive rather than negative after accounting for the year trend. Although we did not find support for the harvest-induced earlier maturation hypothesis, evidence was not clearly in favour of the alternative hypothesis. 4. Our study contrasts results from trophy-hunting traditions targeting large males, and points to a potential role of the cultural tradition. Harvesting in Scandinavia mainly aims for meat targeting calves and yearlings (and males), which is less likely to yield an evolutionary response in maturation of females. Our results, although being on a plastic trait and not directly on genetic make-up, are indicative that harvesting-induced evolution is weak on age at maturation in these populations under the current management regime.

The timing of male reproductive effort relative to female ovulation in a capital breeder.

1. In large herbivores, the timing of breeding is important for females to hit peak plant protein levels. For males, the timing of reproductive effort is important to maximize the number of females they can mate during autumn rut in competition with other males. The latter depends on when most females are ovulating, but also on how other males with a different competitive ability are timing use of their capital (fat); it may pay younger males to invest more heavily later when prime aged males are exhausted. 2. Based on estimates of body mass loss, we quantify how much timing (start, peak and end dates) of male reproductive effort during rutting varies depending on male age, density and climate as well as timing of female ovulation. 3. Ovulation in adult females was delayed by 5 days from low to high density, and ovulation was also more synchronous at high density. The starting date of decline in male body mass was only later in yearlings than among other age groups. However, at low density, peak and end dates of rut became increasingly earlier and close to peak female ovulation with increasing age up to 7 years of age. Prime-aged males matched peak effort closely with peak rate of prime-aged female ovulation, while younger males were delayed. This is consistent with the view that younger males have a better chance when the prime-aged males are becoming exhausted. 4. Apart from yearlings, male age groups were synchronized in both the starting, peak and end dates of mass decline at high density. Thus, this partly follows change in female ovulation patterns, but also suggests that competition among males decreased with increasing density due probably to lower intensity of sexual selection. The lowered sexual selection may be due not only to more synchronous female ovulation, but also increasingly female-biased sex ratios and a younger male age structure with increasing density. 5. The onset of rutting is somewhat independent of male age (apart from the youngest males), but the peak and end of rutting effort is dependent strongly upon age, density and peak female ovulation. Male rutting phenology is thus best interpreted as a compromise between hitting peak female ovulation and intensity of sexual selection.

Hierarchical path analysis of deer responses to direct and indirect effects of climate in northern forest.

A problem in climate studies has been on how to treat causal chains of explanations and both direct and indirect effects. Mammals in strongly seasonal environments of the boreal forest typically lose condition during winter and gain mass (and reproduce) during the summer season when biomass and plant quality peak. Mass decay of large herbivores during winter is due to direct effects of winter weather, such as increased costs of movement, thermoregulation and reduced access to food when snow is deep. Deer condition during summer is thought to be affected mainly indirectly by weather through plants. High spring temperature speeds up plant development, and deep snow can delay phenology in early summer. Current statistical modelling does not take into account these mechanistic pathways. We used hierarchical Bayes modelling to more mechanistically link global climate, local weather and plant phenology to autumn body mass of red deer in Norway. Red deer were much more affected indirectly through trophic interactions. No solid evidence of direct effects of snow depth was found on autumn body mass. We discuss the implications of our results relative to our ability to predict effects of global change on large mammalian herbivores in the boreal forest.

Evidence for a trade-off between early growth and tooth wear in Svalbard reindeer.

Ruminants depend on efficient physical degradation of forage through chewing to increase the surface area of the food particles presented to the microflora. Fossil evidence suggests that increased molar height is an adaptation for wear tolerance in dry ecosystems with sparse vegetation, but no study has shown selection pressure for hypsodonty in contemporary ruminants. We explored the relationships between particle size in rumen, tooth wear (scanned molar occlusal topography), age and body mass of female Svalbard reindeer living in an arctic desert at 78 degrees latitude on Svalbard. We predicted that (H1) if the rumen particle size is determined mainly by constraints due to tooth wear, and if tooth wear is mainly a function of age, average particle size in rumen should increase with age. From allometric relations it is known that larger individuals can survive on a lower-quality diet, we therefore predicted (H2) larger particle sizes with increases in (ln) body mass, irrespective of age and wear. Lastly, if there is a trade-off between growth and tooth wear in dry ecosystems (a selection pressure for hypsodonty), we predicted (H3) that teeth of heavier animals should be more worn than those of lighter animals of the same age. The proportion of small particles (<1.0 mm) decreased rapidly with increasing age (consistent with H1). Heavier females within an age class had more worn teeth (consistent with H3) than lighter ones. A close-to-isometric relationship between particle size and body mass suggested that heavier animals partly compensated for reduced tooth efficiency by chewing more. We provide the first evidence of a trade-off between fast early growth and wear (a somatic cost) of a senescence-related trait--the structure and height of the molar--in a wild ruminant inhabiting an arctic desert where selection pressure for increased tooth height is expected. This suggests that foraging conditions are more extreme than the environment in which the species originally evolved.

Activity pattern of arctic reindeer in a predator-free environment: no need to keep a daily rhythm.

Arctic Cervids face considerable challenges in sustaining life in a harsh and highly seasonal environment, and when to forage is a key component of the survival strategy. We predict that a cervid maximizes net intake of energy to change the duration of feeding-ruminating cycles depending on season, and pays no attention to light or other activity-entraining cues. Still, in periods of bad weather it may pay energetically to reduce exposure and heat loss. We investigated environmental impact on the seasonal and daily activity pattern of a food-limited, predator-free arctic deer, the Svalbard reindeer. We found that the reindeer indeed had season-dependent feeding-rumination intervals, with no distinct peaks in activity at sunrise and sunset, as would be expected if animals maximize energy intake rates in predator-free environments. However, they temporarily reduced activity when exposed to low temperature and increased precipitation during winter, possibly to conserve energy. We provide insight into the behavioural strategy of Svalbard reindeer which enables them to cope with such an extreme environment.

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.

Increased effect of harsh climate in red deer with a poor set of teeth.

Teeth are vital for mammal performance and especially in ungulates relying on mechanical decomposition of plant material for effective microbial digestion and energy uptake. The main focus of the role of teeth in ungulate life histories has been on tooth wear, while no one has addressed to what extent deviation from the natural set of teeth (maldentition) causes variation in individual fitness components. Based on mandibles from 41,066 individual red deer (Cervus elaphus L.) collected from 1969 to 2001, we tested whether maldentition had an effect on individual body condition and whether this effect depended on environmental harshness. Females with maldentition (0.6% of the population) were in a poorer condition than individuals without tooth anomalies and the effect increased during unfavorable climatic conditions. The effect of maldentition in males was less clear. This study indicates that a well-functioning set of teeth is essential for mammal performance, and that selection pressure against (dental) anomalies is more pronounced when climate is unfavorable.

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.

Importance of climatological downscaling and plant phenology for red deer in heterogeneous landscapes.

Understanding how climate influences ecosystems represents a challenge in ecology and natural resource management. Although we know that climate affects plant phenology and herbivore performances at any single site, no study has directly coupled the topography-climate interaction (i.e. the climatological downscaling process) with large-scale vegetation dynamics and animal performances. Here we show how climatic variability (measured by the North Atlantic oscillation 'NAO') interacts with local topography in determining the vegetative greenness (as measured by the normalized difference vegetation index 'NDVI') and the body masses and seasonal movements of red deer (Cervus elaphus) in Norway. Warm springs induced an earlier onset of vegetation, resulting in earlier migration and higher body masses. Increasing values of the winter-NAO corresponded to less snow at low altitude (warmer, more precipitation results in more rain), but more snow at high altitude (colder, more precipitation corresponds to more snow) relative to winters with low winter-NAO. An increasing NAO thus results in a spatially more variable phenology, offering migrating deer an extended period with access to high-quality forage leading to increased body mass. Our results emphasize the importance of incorporating spring as well as the interaction between winter climate and topography when aiming at understanding how plant and animal respond to climate change.

Multiple causes of sexual segregation in European red deer: enlightenments from varying breeding phenology at high and low latitude.

Sexual segregation outside the mating season occurs in most species of sexually dimorphic ungulates and has been extensively described in the literature, but the mechanisms causing segregation are still debated. The detailed pattern of sexual segregation throughout the year has rarely been presented for mammals, and no study, to our knowledge, has used latitudinal-related variation in breeding phenology to shed light on the underlying mechanisms. Recent methodological developments have made it possible to quantify separate components of segregation (social, habitat) and activity synchrony in animal groups, but these major improvements have so far been little used. We observed European red deer year round at two widely different latitudes (France and Norway) and tested three different mechanistic hypotheses of segregation related to: (i) predation risk; (ii) body-size-related forage selection; and (iii) activity budget. Habitat segregation peaked during calving in both populations and dropped rapidly after calving. Females with calves were more segregated from males than were females without calves, pointing to a key role of antipredator behaviour even though large predators are absent in France and extremely rare in Norway. However, at both sites individuals also grouped with their own sex within habitat types (i.e. social segregation), and individuals in mixed-sex groups were less synchronized in activity type than individuals in either unisex male or unisex female groups, suggesting that differences in activity budgets are involved. Social segregation peaked during calving and was lowest during the rut (indicating aggregation) in both populations; these activities occurred one month later in the Northern populations, corresponding well with known differences in breeding phenology. We conclude that latitude-dependent breeding phenology shapes the seasonal pattern of sexual segregation and that sexual segregation in ungulates has multiple causes.

Timing and synchrony of ovulation in red deer constrained by short northern summers.

Iteroparous mothers often face a trade-off between further investments in current offspring at the expense of the start of the next reproductive cycle. In the strongly seasonal environments at northern latitudes, large herbivores are typically calving in early summer each year to get a long growth season and to hit peak protein levels of vegetation. Late-born offspring are more likely to die since they are smaller in autumn. Low female condition in autumn due to prolonged investment in current-year offspring may lower her ability to ovulate sufficiently early to get a good start for the calves the following spring. On the basis of autopsies of uteri from 10,073 red deer (Cervus elaphus), we show that ovulation was delayed as well as more synchronous with increasing population density. This suggests that ovulation beyond a certain date incurs some fitness costs. Ovulation occurs progressively earlier with increasing age up to around 13 yr of age, after which ovulation again occurs later. Low ovulation rates in young compared with prime-aged deer were correlated with late ovulation in the fall. Also, yearling groups with a low rate of ovulation (e.g., because of low weight) also ovulated later, and old senescent deer not calving the previous year ovulated less frequently and markedly later than those raising a calf. Our findings suggest, therefore, that mothers unable to ovulate before a certain date fail to do so altogether that year.

Social rank, feeding and winter weight loss in red deer: any evidence of interference competition?

During winter at northern latitudes, large herbivores often exploit patches of concentrated, relatively high quality forage, which may lead to interference competition. The factors affecting success in contests and subsequent dominance rank, such as age and body weight, remain key issues in ungulate behavioural ecology. Maternal effects on offspring body weight are well known, but few studies have investigated if mother's social rank influence offspring rank. Moreover, no study has related dominance rank in ungulates to weight loss during winter. Outcomes of social interactions (n=7,609), feeding time and spatial position in red deer (Cervus elaphus) hinds and calves, and weight loss of calves, were registered from 1981 to 1996 at six winter-feeding sites within the county of Sør-Trøndelag in Norway. The level of aggressiveness was higher among calves than among adult hinds, and the factors determining the outcome of contests also differed. The initiator won the majority of interactions (more than 90% in both hinds and calves). Social rank was related to both age and body weight in adult hinds, and related to body weight and mother rank in calves. The relationship between feeding time and rank was non-linear. Feeding time was correlated with rank only among high ranked hinds, while there was no such relationship among low ranked hinds or calves. There was no correlation between winter weight loss and social rank in calves. Our study therefore underlines that, although frequent aggression is observed at artificial feeding sites of northern herbivores, this is not necessarily sufficient to give rise to interference competition.

Decelerating and sex-dependent tooth wear in Norwegian red deer.

In ungulates, tooth wear is often suggested as a proximate cause of senescence. Tooth wear is expected to be sex-dependent since energetic requirements and food selection varies largely between sexes in sexually dimorphic ungulates. Furthermore, tooth wear may lower mastication efficiency, and we predict a negative correlation between tooth wear and body weight or condition. We tested these predictions on data on tooth wear (estimated as height of first molar) of 1,311 male and 1,348 female red deer ( Cervus elaphus) aged 3-25 years and harvested along the west coast of Norway. The rate of tooth wear decreased with age. Males wear teeth at a higher rate (from 0.61 mm/year in 4-year olds to 0.45 mm/year in 11-year olds) than females (from 0.52 mm/year in 4-year olds to 0.39 mm/year in 11-year olds). Molar height correlated positively with body weight in both sexes, but not after adjusting for body size. Molar height was strongly dependent on body size in 3-year-old individuals (when tooth wear is minimal). Earlier reports in the literature of a positive correlation between tooth height and body weight may therefore be due to initial size differences rather than differences in condition due to tooth wear.

Age- and density-dependent reproductive effort in male red deer.

Reproductive effort in female ungulates originates from gestation and lactation and has been studied extensively; however, no comparable studies of reproductive effort in males (due to fighting for access to mates) have, to our knowledge, previously been reported. Here, we report on weight loss of male red deer during the annual mating season--a direct measure of male reproductive effort (or somatic reproductive costs). The 'terminal investment' hypothesis predicts that reproductive effort should increase with age, given that costs remain stable. We also propose the 'mating strategy-effort' hypothesis, which predicts that reproductive effort peaks in prime-aged males, since they are most often the harem holders. Consistent with the mating strategy-effort hypothesis, relative weight loss during the rutting season peaked at prime age and was lower in younger and senescent males. Weight loss during the rut was relatively smaller as density increased and more so for older males. This is probably primarily due to males (particularly senescent males) starting their rut in poorer condition at high density. The pattern of reproductive effort in males with regard to age and density therefore differs markedly from the pattern reported for females.

Extrinsic Modification of Vertebrate Sex Ratios by Climatic Variation.

Evidence for the influences of climate on early development, maternal condition, and offspring viability in terrestrial vertebrates suggests that climatic change has the potential to induce variation in offspring sex ratios in such organisms. Using long-term data at individual and population levels, we investigated the influence of global climatic variation, as a result of the North Atlantic Oscillation (NAO), on offspring sex ratios of red deer in Norway. The state of the NAO during the fetal development of hinds influenced the mass of their sons, but not daughters, and increasingly warmer and snowy winters led to increasingly male-biased offspring sex ratios, independently of changes in the mean age of hinds. Moreover, hinds that were themselves born following warm, snowy winters were smaller as adults, produced significantly lighter sons, and tended to produce more sons than hinds born following cold, dry winters. In light of the fact that these observations defy explanation according to previous hypotheses of adaptive modification of offspring sex ratios, we present the extrinsic modification hypothesis, which suggests that sex ratios may evolve in variable environments through natural selection independently of maternal strategies of sex allocation.