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.     

Parameterization and validation of an ungulate‐pasture model

Ungulate grazing and trampling strongly affect pastures and ecosystems throughout the world. Ecological population models are used for studying these systems and determining the guidelines for sustainable and economically viable management. However, the effect of trampling and other resource wastage is either not taken into account or quantified with data in earlier models. Also, the ability of models to describe the herbivore impact on pastures is usually not validated. We used a detailed model and data to study the level of winter‐ and summertime lichen wastage by reindeer and the effects of wastage on population sizes and management. We also validated the model with respect to its ability of predicting changes in lichen biomass and compared the actual management in herding districts with model results. The modeling efficiency value (0.75) and visual comparison between the model predictions and data showed that the model was able to describe the changes in lichen pastures caused by reindeer grazing and trampling. At the current lichen biomass levels in the northernmost Finland, the lichen wastage varied from 0 to 1 times the lichen intake during winter and from 6 to 10 times the intake during summer. With a higher value for wastage, reindeer numbers and net revenues were lower in the economically optimal solutions. Higher wastage also favored the use of supplementary feeding in the optimal steady state. Actual reindeer numbers in the districts were higher than in the optimal steady‐state solutions for the model in 18 herding districts out of 20. Synthesis and applications. We show that a complex model can be used for analyzing ungulate‐pasture dynamics and sustainable management if the model is parameterized and validated for the system. Wastage levels caused by trampling and other causes should be quantified with data as they strongly affect the results and management recommendations. Summertime lichen wastage caused by reindeer is higher than expected, which suggests that seasonal pasture rotation should be used to prevent the heavy trampling of winter lichen pastures during summer. In the present situation, reindeer numbers in northernmost Finland are in most cases higher than in the management solutions given by the model.     

Use of climatic data to assess the effect of insect harassment on the autumn weight of reindeer (Rangifer tarandus) calves

Considerable behavioural evidence supports harassment by insects as the most important causal link between warm summer temperatures and low body condition of reindeer Rangifer tarandus , and that insect activity is influenced by weather condition. However, much less is known about the effect of insect harassment on individual performance, measured as reduced weight gain during summer, and the related consequences on both the reindeer pastoral economy and reindeer as a biological resource. Using climatic data, this paper develops a simple index for the analysis of insect harassment that takes into consideration weather variables known to significantly affect insect activity and/or the level of insect harassment. The insect harassment index, which is based on mid-day ambient temperature ≥13 °C, wind speed <6 m/s and cloud cover <40%, is further used to test the hypothesis that insect harassment has a negative effect on reindeer performance during summer in three Norwegian populations. Results show that harassment by insects negatively affects the autumn weight of reindeer calves, most probably through reduced grazing time and increased energy expenditure, but also indirectly by negatively influencing milk production of the dam. Moreover, female calves were more vulnerable to insect harassment than males. Insect harassment may have consequences on future reproductive performance, calving time, calf birth weight and hence neonatal mortality, and thus affect reindeer productivity. The presented index is easy to estimate and may be used to quantify and compare harassment levels on various reindeer summer grazing areas for management purposes. Our results also suggest that the expected temperature increase in the course of global warming may increase the insect-related stress on reindeer.     

Complex biotic interactions drive long-term vegetation dynamics in a subarctic ecosystem

Predicting impacts of global warming requires understanding of the extent to which plant biomass and production are controlled by bottom-up and top-down drivers. By annually monitoring community composition in grazed control plots and herbivore-free exclosures at an Arctic location for 15 years, we detected multiple biotic interactions. Regular rodent cycles acted as pulses driving synchronous fluctuations in the biomass of field-layer vegetation; reindeer influenced the biomass of taller shrubs, and the abundance of plant pathogenic fungi increased when densities of their host plants increased in exclosures. Two outbreaks of geometrid moths occurred during the study period, with contrasting effects on the field layer: one in 2004 had marginal effects, while one in 2012 severely reduced biomass in the control plots and eliminated biomass that had accumulated over 15 years in the exclosures. The latter was followed by a dramatic decline of the dominant understory dwarf-shrub Empetrum hermaphroditum, driven by an interaction between moth herbivory on top buds and leaves, and increased disease severity of a pathogenic fungus. We show that the climate has important direct and indirect effects on all these biotic interactions. We conclude that long time series are essential to identify key biotic interactions in ecosystems, since their importance will be influenced by climatic conditions, and that manipulative treatments are needed in order to obtain the mechanistic understanding needed for robust predictions of future ecosystem changes and their feedback effects.     

Polymorphisms and variants in the prion protein sequence of European moose (Alces alces), reindeer (Rangifer tarandus), roe deer (Capreolus capreolus) and fallow deer (Dama dama) in Scandinavia

The prion protein (PrP) sequence of European moose, reindeer, roe deer and fallow deer in Scandinavia has high homology to the PrP sequence of North American cervids. Variants in the European moose PrP sequence were found at amino acid position 109 as K or Q. The 109Q variant is unique in the PrP sequence of vertebrates. During the 1980s a wasting syndrome in Swedish moose, Moose Wasting Syndrome (MWS), was described. SNP analysis demonstrated a difference in the observed genotype proportions of the heterozygous Q/K and homozygous Q/Q variants in the MWS animals compared with the healthy animals. In MWS moose the allele frequencies for 109K and 109Q were 0.73 and 0.27, respectively, and for healthy animals 0.69 and 0.31. Both alleles were seen as heterozygotes and homozygotes. In reindeer, PrP sequence variation was demonstrated at codon 176 as D or N and codon 225 as S or Y. The PrP sequences in roe deer and fallow deer were identical with published GenBank sequences.     

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

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

Allometry and variability of resource allocation to reproduction in a wild reindeer population

The differential allocation of energy to either reproductionor survival represents a major conflict with important implicationsfor patterns of life history. Here, we explore how covariationbetween maternal body weight and fetal weight vary accordingto fetal sex in a wild reindeer (Rangifer tarandus) populationduring two contrasting years. Maternal weights differed duringthe 2 years, probably because of a difference in populationdensity. We could not detect any change in the allocation toreproduction depending on female phenotypic distribution. Malefetuses were heavier than female fetuses, with the same relativedimorphism in both years. There was no support for a correlationbetween the sex of the fetus carried by a female and her weight.Our results suggest that the level of resource allocation toreproduction during the prenatal period is strongly determinedby female body weight and the allometric relationship betweenbody weight and metabolic rate. We discuss the consequencesof our results for population dynamics. We call for an integrationof inter- and intraspecific allometric approaches to betterunderstand constraints and variation in life-history traits.     

Herbivore grazing—or trampling? Trampling effects by a large ungulate in cold high‐latitude ecosystems

Mammalian herbivores have important top‐down effects on ecological processes and landscapes by generating vegetation changes through grazing and trampling. For free‐ranging herbivores on large landscapes, trampling is an important ecological factor. However, whereas grazing is widely studied, low‐intensity trampling is rarely studied and quantified. The cold‐adapted northern tundra reindeer (Rangifer tarandus) is a wide‐ranging keystone herbivore in large open alpine and Arctic ecosystems. Reindeer may largely subsist on different species of slow‐growing ground lichens, particularly in winter. Lichen grows in dry, snow‐poor habitats with frost. Their varying elasticity makes them suitable for studying trampling. In replicated factorial experiments, high‐resolution 3D laser scanning was used to quantify lichen volume loss from trampling by a reindeer hoof. Losses were substantial, that is, about 0.3 dm³ per imprint in dry thick lichen, but depended on type of lichen mat and humidity. Immediate trampling volume loss was about twice as high in dry, compared to humid thin (2–3 cm), lichen mats and about three times as high in dry vs. humid thick (6–8 cm) lichen mats, There was no significant difference in volume loss between 100% and 50% wetted lichen. Regained volume with time was insignificant for dry lichen, whereas 50% humid lichen regained substantial volumes, and 100% humid lichen regained almost all lost volume, and mostly within 10–20 min. Reindeer trampling may have from near none to devastating effects on exposed lichen forage. During a normal week of foraging, daily moving 5 km across dry 6‐ to 8‐cm‐thick continuous lichen mats, one adult reindeer may trample a lichen volume corresponding to about a year's supply of lichen. However, the lichen humidity appears to be an important factor for trampling loss, in addition to the extent of reindeer movement.     

Refugial origins of reindeer (Rangifer tarandus L.) inferred from mitochondrial DNA sequences

The glacial-interglacial cycles of the upper Pleistocene have had a major impact on the recent evolutionary history of Arctic species. To assess the effects of these large-scale climatic fluctuations to a large, migratory Arctic mammal, we assessed the phylogeography of reindeer (Rangifer tarandus) as inferred from mitochondrial DNA (mtDNA) sequence variation in the control region. Phylogenetic relationships among haplotypes seem to reflect historical patterns of fragmentation and colonization rather than clear-cut relationships among extant populations and subspecies. Three major haplogroups were detected, presumably representing three separate populations during the last glacial. The most influential one has contributed to the gene pool of all extant subspecies and seems to represent a large and continuous glacial population extending from Beringia and far into Eurasia. A smaller, more localized refugium was most likely isolated in connection with ice expansion in western Eurasia. A third glacial refugium was presumably located south of the ice sheet in North America, possibly comprising several separate refugial populations. Significant demographic population expansion was detected for the two haplogroups representing the western Eurasian and Beringian glacial populations. The former apparently expanded when the ice cap retreated by the end of the last glacial. The large continuous one, in contrast, seems to have expanded by the end of the last interglacial, indicating that the warm interglacial climate accompanied by marine transgression and forest expansion significantly confined population size on the continental mainland. Our data demonstrate that the current subspecies designation does not reflect the mtDNA phylogeography of the species, which in turn may indicate that morphological differences among subspecies have evolved as adaptive responses to postglacial environmental change.