Arctic animals inhabit some of the coldest environments on the planet and have evolved physiological mechanisms for minimizing heat loss under extreme cold. However, the Arctic is warming faster than the global average and how well Arctic animals tolerate even moderately high air temperatures (Ta) is unknown. Using flow‐through respirometry, we investigated the heat tolerance and evaporative cooling capacity of snow buntings (Plectrophenax nivalis; ≈31 g, N = 42), a cold specialist, Arctic songbird. We exposed buntings to increasing Ta and measured body temperature (Tb), resting metabolic rate (RMR), rates of evaporative water loss (EWL), and evaporative cooling efficiency (the ratio of evaporative heat loss to metabolic heat production). Buntings had an average (±SD) Tb of 41.3 ± 0.2°C at thermoneutral Ta and increased Tb to a maximum of 43.5 ± 0.3°C. Buntings started panting at Ta of 33.2 ± 1.7°C, with rapid increases in EWL starting at Ta = 34.6°C, meaning they experienced heat stress when air temperatures were well below their body temperature. Maximum rates of EWL were only 2.9× baseline rates at thermoneutral Ta, a markedly lower increase than seen in more heat‐tolerant arid‐zone species (e.g., ≥4.7× baseline rates). Heat‐stressed buntings also had low evaporative cooling efficiencies, with 95% of individuals unable to evaporatively dissipate an amount of heat equivalent to their own metabolic heat production. Our results suggest that buntings’ well‐developed cold tolerance may come at the cost of reduced heat tolerance. As the Arctic warms, and this and other species experience increased periods of heat stress, a limited capacity for evaporative cooling may force birds to increasingly rely on behavioral thermoregulation, such as minimizing activity, at the expense of diminished performance or reproductive investment.

No abstract

Cold acclimatization (phenotypic adjustments to cope with cold conditions) is an imperative requirement for birds living at high latitudes during the cold depths of winter. Despite the significant remodelling of key phenotypic traits and energetic costs associated with elevating cold endurance, winter cold acclimatization can also provide further carryover benefits to subsequent stages in species wintering, migrating and breeding in cold environments (e.g. the Arctic). We tested this beneficial carryover hypothesis using outdoor captive Arctic‐breeding snow buntings Plectrophenax nivalis, a cold specialist known for its impressive wintering thermogenic capabilities. We compared changes in phenotypic traits supporting cold acclimatization—body composition (body, fat, lean mass, pectoral muscle thickness), oxygen carrying capacity (haematocrit), thermogenic capacity and endurance (Msum, time to Msum), cold tolerance (Ta at Msum) and maintenance energy expenditure (BMR)—between the wintering, migratory and arrival/summer stages. Body mass (+31%), fat mass (+226%) and BMR (+13%) increased relative to the winter phenotype, likely to support the added costs of migration—that is the migratory upregulation hypothesis. In contrast, lean mass, pectoral muscle thickness, haematocrit and thermogenic capacity remained high and stable at winter level across stages in support of the thermal carryover hypothesis. The maintenance of these traits likely offers spare capacity for unpredictable cold environments expected during migration and breeding in the Arctic. Our results thus suggest that birds can extend the long‐term advantages of winter phenotypic adjustments through additional benefits to thermogenic capacity during subsequent life‐history stages. These benefits likely make it possible for Arctic‐breeding birds to maximize success across diverse life‐history stages in the face of extreme cold conditions.

Phenotypic flexibility has received considerable attention in the last decade; however, whereas many studies have reported amplitude of variation in phenotypic traits, much less attention has focused on the rate at which traits can adjust in response to sudden changes in the environment. We investigated whole animal and muscle phenotypic changes occurring in black-capped chickadees ( Poecile atricapillus) acclimated to cold (−5°C) and warm (20°C) temperatures in the first 3 h following a 15°C temperature drop (over 3 h). Before the temperature change, cold-acclimated birds were consuming 95% more food, were carrying twice as much body fat, and had 23% larger pectoralis muscle fiber diameters than individuals kept at 20°C. In the 3 h following the temperature drop, these same birds altered their pectoralis muscle ultrastructure by increasing the number of capillaries per fiber area and the number of nuclei per millimeter of fiber by 22%, consequently leading to a 22% decrease in myonuclear domain (amount of cytoplasm serviced per nucleus), whereas no such changes were observed in the warm-acclimated birds. To our knowledge, this is the first demonstration of such a rapid adjustment in muscle fiber ultrastructure in vertebrates. These results support the hypothesis that chickadees maintaining a cold phenotype are better prepared than warm-phenotype individuals to respond to a sudden decline in temperature, such as what may be experienced in their natural wintering environment.