An arctic breeding songbird overheats during intense activity even at low air temperatures.

Birds maintain some of the highest body temperatures among endothermic animals. Often deemed a selective advantage for heat tolerance, high body temperatures also limits birds' thermal safety margin before reaching lethal levels. Recent modelling suggests that sustained effort in Arctic birds might be restricted at mild air temperatures, which may require reductions in activity to avoid overheating, with expected negative impacts on reproductive performance. We measured within-individual changes in body temperature in calm birds and then in response to an experimental increase in activity in an outdoor captive population of Arctic, cold-specialised snow buntings (Plectrophenax nivalis), exposed to naturally varying air temperatures (- 15 to 36 °C). Calm buntings exhibited a modal body temperature range from 39.9 to 42.6 °C. However, we detected a significant increase in body temperature within minutes of shifting calm birds to active flight, with strong evidence for a positive effect of air temperature on body temperature (slope = 0.04 °C/ °C). Importantly, by an ambient temperature of 9 °C, flying buntings were already generating body temperatures ≥ 45 °C, approaching the upper thermal limits of organismal performance (45-47 °C). With known limited evaporative heat dissipation capacities in these birds, our results support the recent prediction that free-living buntings operating at maximal sustainable rates will increasingly need to rely on behavioural thermoregulatory strategies to regulate body temperature, to the detriment of nestling growth and survival.

Born in the cold: contrasted thermal exchanges and maintenance costs in juvenile and adult snow buntings on their breeding and wintering grounds.

Several species of passerines leave their nest with unfinished feather growth, resulting in lower feather insulation and increased thermoregulatory demands compared to adults. However, feather insulation is essential for avian species breeding at northern latitudes, where cold conditions or even snowstorms can occur during the breeding season. In altricial arctic species, increased heat loss caused by poor feather insulation during growth could be counter-adaptative as it creates additional energy demands for thermoregulation. Using flow-through respirometry, we compared resting metabolic rate at thermoneutrality (RMRt), summit metabolic rate (Msum) and heat loss (conductance) in adult and juvenile snow buntings on their summer and winter grounds. In summer, when buntings are in the Arctic, juveniles had a 12% higher RMRt, likely due to unfinished growth, and lost 14% more heat to the environment than adults. This pattern may result from juveniles fledging early to avoid predation at the cost of lower feather insulation. Surprisingly, an opposite pattern was observed at lower latitudes on their wintering grounds. Although they showed no difference in RMRt and Msum, adults were losing 12% more heat than juveniles. We suggest that this difference is due to poorer insulative property of plumage in adults stemming from energetic and time constraints encountered during their post-breeding molt. High plumage insulation in first-winter juvenile buntings could be adaptive to reduce thermoregulatory demands and maximize survival in the first winter of life, while adults could use behavioral strategies to compensate for their greater rate of heat loss.

Warming in the land of the midnight sun: breeding birds may suffer greater heat stress at high- versus low-Arctic sites.

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.

Limited heat tolerance in a cold-adapted seabird: implications of a warming Arctic.

The Arctic is warming at approximately twice the global rate, with well-documented indirect effects on wildlife. However, few studies have examined the direct effects of warming temperatures on Arctic wildlife, leaving the importance of heat stress unclear. Here, we assessed the direct effects of increasing air temperatures on the physiology of thick-billed murres (Uria lomvia), an Arctic seabird with reported mortalities due to heat stress while nesting on sun-exposed cliffs. We used flow-through respirometry to measure the response of body temperature, resting metabolic rate, evaporative water loss and evaporative cooling efficiency (the ratio of evaporative heat loss to metabolic heat production) in murres while experimentally increasing air temperature. Murres had limited heat tolerance, exhibiting: (1) a low maximum body temperature (43.3°C); (2) a moderate increase in resting metabolic rate relative that within their thermoneutral zone (1.57 times); (3) a small increase in evaporative water loss rate relative that within their thermoneutral zone (1.26 times); and (4) a low maximum evaporative cooling efficiency (0.33). Moreover, evaporative cooling efficiency decreased with increasing air temperature, suggesting murres were producing heat at a faster rate than they were dissipating it. Larger murres also had a higher rate of increase in resting metabolic rate and a lower rate of increase in evaporative water loss than smaller murres; therefore, evaporative cooling efficiency declined with increasing body mass. As a cold-adapted bird, murres' limited heat tolerance likely explains their mortality on warm days. Direct effects of overheating on Arctic wildlife may be an important but under-reported impact of climate change.

Poor prey quality is compensated by higher provisioning effort in passerine birds.

In altricial avian species, nutrition can significantly impact nestling fitness by increasing their survival and recruitment chances after fledging. Therefore, the effort invested by parents towards provisioning nestlings is crucial and represents a critical link between habitat resources and reproductive success. Recent studies suggest that the provisioning rate has little or no effect on the nestling growth rate. However, these studies do not consider prey quality, which may force breeding pairs to adjust provisioning rates to account for variation in prey nutritional value. In this 8-year study using black-capped (Poecile atricapillus) and boreal (Poecile hudsonicus) chickadees, we hypothesized that provisioning rates would negatively correlate with prey quality (i.e., energy content) across years if parents adjust their effort to maintain nestling growth rates. The mean daily growth rate was consistent across years in both species. However, prey energy content differed among years, and our results showed that parents brought more food to the nest and fed at a higher rate in years of low prey quality. This compensatory effect likely explains the lack of relationship between provisioning rate and growth rate reported in this and other studies. Therefore, our data support the hypothesis that parents increase provisioning efforts to compensate for poor prey quality and maintain offspring growth rates.

Limited heat tolerance in an Arctic passerine: Thermoregulatory implications for cold-specialized birds in a rapidly warming world.

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 (T a) 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 T a and measured body temperature (T b), 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) T b of 41.3 ± 0.2°C at thermoneutral T a and increased T b to a maximum of 43.5 ± 0.3°C. Buntings started panting at T a of 33.2 ± 1.7°C, with rapid increases in EWL starting at T a = 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 T a, 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.

Wintering Snow Buntings Elevate Cold Hardiness to Extreme Levels but Show No Changes in Maintenance Costs.

AbstractResident 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.

Avian thermoregulation in the heat: is evaporative cooling more economical in nocturnal birds?

Evaporative cooling is a prerequisite for avian occupancy of hot, arid environments, and is the only avenue of heat dissipation when air temperatures (Ta) exceed body temperature (Tb). Whereas diurnal birds can potentially rehydrate throughout the day, nocturnal species typically forgo drinking between sunrise and sunset. We hypothesized that nocturnal birds have evolved reduced rates of evaporative water loss (EWL) and more economical evaporative cooling mechanisms compared with diurnal species, permitting nocturnal species to tolerate extended periods of intense heat without becoming lethally dehydrated. We used phylogenetically informed regressions to compare EWL and evaporative cooling efficiency [ratio of evaporative heat loss (EHL) and metabolic heat production (MHP); EHL/MHP] among nocturnal and diurnal birds at high Ta We analyzed variation in three response variables: (1) slope of EWL at Ta between 40 and 46°C, (2) EWL at Ta=46°C and (3) EHL/MHP at Ta=46°C. Nocturnality emerged as a weak, negative predictor, with nocturnal species having slightly shallower slopes and reduced EWL compared with diurnal species of similar mass. In contrast, nocturnal activity was positively correlated with EHL/MHP, indicating a greater capacity for evaporative cooling in nocturnal birds. However, our analysis also revealed conspicuous differences among nocturnal taxa. Caprimulgids and Australian owlet-nightjars had shallower slopes and reduced EWL compared with similarly sized diurnal species, whereas owls had EWL rates comparable to those of diurnal species. Consequently, our results did not unequivocally demonstrate more economical cooling among nocturnal birds. Owls predominately select refugia with cooler microclimates, but the more frequent and intense heat waves forecast for the 21st century may increase microclimate temperatures and the necessity for active heat dissipation, potentially increasing owls' vulnerability to dehydration and hyperthermia.

Avian thermoregulation in the heat: efficient evaporative cooling in two southern African nightjars.

Nightjars represent a model taxon for investigating physiological limits of heat tolerance because of their habit of roosting and nesting in sunlit sites during the heat of the day. We investigated the physiological responses of Rufous-cheeked nightjars (Caprimulgus rufigena) and Freckled nightjars (Caprimulgus tristigma) to high air temperatures (T a) by measuring body temperature (T b), resting metabolic rate (RMR) and total evaporative water loss (TEWL) at T a ranging from 10 to 56 °C. Both species became hyperthermic at T a > T b. Lower critical limits of thermoneutrality occurred at T a between 35 and 37 °C, whereas we detected no clear upper critical limits of thermoneutrality. Between T a ≈ 37.0 and 39.9 °C, rates of TEWL increased rapidly with T a. At T a ≥ 40 °C, fractional increases in mass-specific TEWL rates were 78-106% of allometric predictions. Increasing evaporative heat dissipation incurred only small metabolic costs, with the RMR of neither species ever increasing by more than 20% above thermoneutral values. Consequently, both species displayed extremely efficient evaporative cooling; maximum evaporative heat dissipation was equivalent to 515% of metabolic heat production (MHP) at T a ≈ 56 °C in C. rufigena and 452% of MHP at T a ≈ 52 °C in C. tristigma. Our data reiterate that caprimulgids have evolved an efficient mechanism of evaporative cooling via gular fluttering, which minimizes metabolic heat production at high T a and reduces total heat loads. This likely aids in reducing TEWL rates and helps nightjars cope with some of the most thermally challenging conditions experienced by any bird.