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Rising global temperatures are expected to increase reproductive costs for wildlife as greater thermoregulatory demands interfere with reproductive activities. However, predicting the temperatures at which reproductive performance is negatively impacted remains a significant hurdle. Using a thermoregulatory polygon approach, we derived a reproductive threshold temperature for an Arctic songbird—the snow bunting ( Plectrophenax nivalis ). We defined this threshold as the temperature at which individuals must reduce activity to suboptimal levels (i.e. less than four-time basal metabolic rate) to sustain nestling provisioning and avoid overheating. We then compared this threshold to operative temperatures recorded at high (82° N) and low (64° N) Arctic sites to estimate how heat constraints translate into site-specific impacts on sustained activity level. We predict buntings would become behaviourally constrained at operative temperatures above 11.7°C, whereupon they must reduce provisioning rates to avoid overheating. Low-Arctic sites had larger fluctuations in solar radiation, consistently producing daily periods when operative temperatures exceeded 11.7°C. However, high-latitude birds faced entire, consecutive days when parents would be unable to sustain required provisioning rates. These data indicate that Arctic warming is probably already disrupting the breeding performance of cold-specialist birds and suggests counterintuitive and severe negative impacts of warming at higher latitude breeding locations.

Neonicotinoids are insecticides widely used as seed treatments that appear to have multiple negative effects on birds at a diversity of biological scales. Adult birds exposed to a low dose of imidacloprid, one of the most commonly used neonicotinoids, presented reduced fat stores, delayed migration and potentially altered orientation. However, little is known on the effect of imidacloprid on birds growth rate despite studies that have documented disruptive effects of low imidacloprid doses on thyroid gland communication. We performed a $$2 \times 2$$ 2 × 2 factorial design experiment in Zebra finches, in which nestling birds were exposed to a very low dose (0.205 mg kg body $$\hbox {mass}^{-1}$$ mass - 1 ) of imidacloprid combined with food restriction during posthatch development. During the early developmental period, imidacloprid exposure resulted in an improvement of body condition index in treated nestlings relative to controls. Imidacloprid also led to compensatory growth in food restricted nestlings. This early life neonicotinoid exposure also carried over to adult age, with exposed birds showing higher lean mass and basal metabolic rate than controls at ages of 90–800 days. This study presents the first evidence that very low-dose neonicotinoid exposure during early life can permanently alter adult phenotype in birds.

Rising global temperatures are expected to increase reproductive costs for wildlife as greater thermoregulatory demands interfere with essential breeding activities such as parental care. However, predicting the temperature threshold where reproductive performance is negatively impacted remains a significant hurdle. Using a novel thermoregulatory polygon approach, we predicted the threshold temperature at which an Arctic songbird–the snow bunting (Plectrophenax nivalis)–would need to reduce activity and perform below the 4-times basal metabolic rate (BMR) required to sustain nestling provisioning to avoid overheating. We then compared this threshold to operative temperatures recorded at high (82°N) and low (64°N) Arctic sites to estimate how heat constraints translate into site-specific impacts on sustained activity level. We predict buntings would become behaviourally constrained at operative temperatures above 11.7°C, whereupon they must reduce provisioning rates to maintain thermal balance. Low Arctic sites had larger fluctuations in solar radiation, producing consistent daily periods when operative temperatures exceeded 11.7°C. However, high-latitude birds faced entire, consecutive days where parents would not be able to sustain required provisioning rates. These data indicate that Arctic warming is likely already disrupting the breeding performance of cold-specialist birds, but also suggests counterintuitive and severe negative impacts of warming at high-latitude breeding locations.

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.

In long-distance migrants, preparation for migration is typically associated with increases in fat and body mass, and with an enlargement of pectoralis muscle mass that likely improves flight performance. Although changes in muscle mass or size have been well described in migratory birds, potential changes in muscle ultrastructure during this transition still deserves scrutiny. Using outdoor captive snow buntings (Plectrophenax nivalis n = 15) measured during their transition into a spring migratory phenotype as a model system, we studied changes in pectoralis muscle ultrastructure and predicted that muscle fiber diameter could increase in parallel with the gain in body mass. We also expected that larger fibers could either recruit satellite cells to support cellular maintenance and protein turnover, increase myonuclear domain (cytoplasm per nuclei) with a potential increase in protein turnover load per myonucleus, or existing myonuclei could undergo endoreduplication. Buntings increased body mass by 46% within a month, largely due to a > 6-fold increase in body fat. However, this increase in body mass was also associated with a 36% increase in muscle fiber diameter. Both pectoralis muscle mass (r2 = 0.57–0.77) and fiber diameter (r2 = 0.32) correlated with total body mass, without any change in the number of nuclei per fiber. Consequently, variation in myonuclear domain (i.e. the amount of cytoplasm per nucleus), was also positively associated with body mass (r2 = 0.51). Therefore, buntings preparing for migration may experience an increase in muscle contraction force due to larger muscle fibers, but this is also coupled with increases in myonuclear domain, which may force these cells to increase protein production to safeguard satellite cells.

Resident temperate passerines adjust their phenotypes to cope with winter constraints, with peak performance in metabolic traits typically occurring during the coldest months. However, it is sparsely known whether cold-adapted northern species make similar adjustments when faced with variable seasonal environments. Life in near-constant cold could be associated with limited flexibility in traits underlying cold endurance. We investigated this by tracking individual physiological changes over five consecutive winters in snow buntings (Plectrophenax nivalis), an Arctic-breeding migratory passerine typically confronted with nearly constant cold. Buntings were held in an outdoor aviary and exposed to seasonal temperature variation typical of temperate zone climates. We measured phenotypic changes in body composition (body, fat, and lean mass, pectoralis muscle thickness), oxygen transport capacity (hematocrit), metabolic performance (basal metabolic rate [BMR] and summit metabolic rate [Msum]), thermogenic endurance (time to reach Msum), and cold tolerance (temperature at Msum). Snow buntings showed flexibility in functions underlying thermogenic capacity and cold endurance comparable to that observed in temperate resident passerines wintering at similar latitudes. Specifically, they increased body mass (13%), fat mass (246%), hematocrit (23%), pectoralis muscle thickness (8%), and Msum (27%). We also found remarkable cold tolerance in these birds, with individuals reaching Msum in helox at temperatures equivalent to less than -90°C in air. However, in contrast with resident temperate passerines, lean mass decreased by 12%, and there was no clear increase in maintenance costs (BMR). Our results show that the flexibility of traits underlying thermal acclimatization in a cold-adapted northern species is comparable to that of temperate resident species living at lower latitudes and is therefore not limited by life in near-constant cold.

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.

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.

Seasonal changes in maximal thermogenic capacity (Msum) in wild black-capped chickadees suggests that adjustments in metabolic performance are slow and begin to take place before winter peaks. However, when mean minimal ambient temperature (Ta) reaches -10°C, chickadee's phenotype appears to provide enough spare capacity to endure days with colder Tas, down to -20°C or below. This suggests that birds could also maintain a higher antioxidant capacity as part of their cold acclimated phenotype to deal with sudden decreases in temperature. Here, we tested how environmental mismatch affected oxidative stress by comparing cold acclimated (-5°C) and transition phenotypes (20°C) in chickadees exposed to an acute 15°C drop in temperature to that of control individuals. We measured superoxide dismutase, catalase, and glutathione peroxidase activities, as well as lipid peroxidation damage, and antioxidant scavenging capacity in pectoralis muscle, brain, intestine and liver. We generally found differences between seasonal phenotypes and across tissues, but no differences with respect to an acute cold drop treatment. Our data suggest oxidative stress is closely matched to whole-animal physiology in cold-acclimated birds compared with transition birds, implying that changes to the oxidative stress system happen slowly.