Trapped in a cold-adapted body: the causes and consequences of phenotypic change in a rapidly warming Arctic

The ability to adapt to rapid climate change is possibly the most important contemporary topic in ecology. Svalbard is a climate change hotspot where we have investigated effects of climate change on the physiology, behaviour and population dynamics of Svalbard reindeer. Our study was the first to measure the metabolic rate of free-ranging wild individuals. From earlier captive studies, we expected to find very low metabolic rates in winter due to extreme energy conservation. Using the doubly labelled (isotope) water technique over a 14-day period, we were surprised to find that the field metabolic rate (including activity) was lower than the previously recorded resting metabolic rate in captivity. The field metabolic rate (FMR) was as low as lama, panda and three species of marsupials, all species known from the scientific literature to have extraordinarily low metabolism. However, we cannot label Svalbard reindeer as ?standing hibernators? because the FMR was three times higher than a winter-sleeping brown bear. We estimated that an adult female reindeer would need to cover 2/3 of their winter energy demands from foraging, but that this ratio depended strongly on the stored fat level accumulated in the preceding autumn. The same individuals were fitted with heart rate loggers, which revealed that Svalbard reindeer is a world record holder among ungulates in the seasonal amplitude of heart rate, increasing from a mean 40 beats per minute in winter to more than 100 in summer. Surprisingly, there was little difference between resting and active heart rate in summer. The resting pulse of nearly 100 in summer signifies a strong time constraint, where digestion, lactation and recovery of body reserves all occur over a few weeks in the short Arctic summer. Since a high metabolic rate can increase the risk of overheating in summer, we investigated behavioural thermoregulation strategies. Reindeer spend a large part of the day ruminating and we predicted they would select warm bed sites on cold days and cold bed sites on warm days. We found support for this since reindeer started selecting cold bed sites when ambient temperatures rose above 9 ºC. An important aspect of climate change is the altered seasonality with longer summers and shorter winters. Many studies have focused on the earlier springs, but the role of later autumns has been comparatively neglected. Using daily predicted snow maps and locations from GPS-marked animals, we quantified if each individual experienced early or late snow fall. We found that timing of early snow between years differed by one month, mainly caused by variation between years. Individuals experiencing late snow fall were 5 kg (10%) heavier than individuals experiencing early snow, a weight difference which dramatically affects the probability of successful reproduction. This positive autumn effect has counteracted the negative effect of icy winters and is the likely cause of the overall population increase. Through detailed life history studies, we have investigated how warmer autumns and icy winters affects individual fitness. First, we explored how being born after good versus bad years (cohort effects) affects performance later in life and, second, the cost of reproduction. We found marked cohort effects reproductive success only in average years, because ?all? individuals reproduce under good conditions and ?none? under harsh conditions (Pigeon et al 2019). The cost of reproduction on the probability of producing a calf next year was affected by the same environmental variables. During the project we have acquired new knowledge on the effects of climate change on Svalbard reindeer. Our reindeer study population has increased 2-3 fold during the last 25 years, with warner autumns and later snow the likely main contributor. This is corroborated by the physiological study: most of the winter energy needs are covered by foraging and not fat. Later snow fall may delay the switch from fat accumulation to depletion, thereby increasing survival and reproduction. Thus, we have downplayed the role of icy winters and increased the attention of shortening of the winter as a main positive factor. Also, contributing to this view is work showing that the population has an ability for rapid recover from icy winters because the most robust component of the population (prime aged females) have high reproductive and survival performance in years following harsh winters. Nevertheless, we also found early warning signals that Svalbard reindeer may be sensitive to continued rising summer temperatures. The high and constant heart rate in summer, even when resting, suggests that they are close to a physiological ceiling set by the ability to dissipate heat. The low ambient temperature threshold for selecting cool bed sites substantiates that increasing summer heat could become an important future driver of reindeer physiology, behaviour and population dynamics.

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Quantifying species vulnerability to climate change is a major challenge. Adaptive responses to climate change can be rapid through phenotypic changes in behaviour, morphology and life history, changes that may only partly have a genetic component. A shrinking of body size has recently been reported as a global phenomenon in response to climate change. Although believed to reflect altered energetic needs, the mechanisms and the individual to population level consequences of shrinking remains poorly understood. Our study will integrate metabolic and evolutionary theories to identify the physiological, behavioural, life-history and demographic consequences of shrinking body size using wild Svalbard reindeer as a case study, a keystone species in the rapidly warming Arctic. We will quantify the effect of body size on individual physiology, associated behavioural strategies and the fitness contribution of animals of varying body size in relation to climate. The proposal builds on a 22-year long individual-based study, which will expand into the field of ecophysiology. We will investigate phenotypic plasticity asking whether small sized animals are better physiologically adapted to all aspects of the warmer environment, or if energy conservation in winter and constraints on heat dissipation in summer cause contrasting selection pressure on size. Already, we have piloted the acquisition of physiological data in our study using heart rate, body temperature and activity telemetry. Now we will corroborate field measurements by direct estimates of metabolic rate using doubly labelled water. In addition, we will explore potential resilience strategies based on adaptive behavioural adjustments of space use and adjustment of life-history strategies. The research will produce novel insights into the mechanisms behind and implications of the widespread phenomena of shrinking in animal body size, and make a fundamental contribution to ecological research on climate change impacts.