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Synopsis Endothermic species have evolved strategies to maximize survival in highly variable or extreme environments. Birds are exemplary as they are among the most widely distributed endotherms on the planet, living in all manner of inhospitable environments. As an example, winter in temperate regions is characterized by cold temperatures and low food availability. Some birds have evolved to tolerate these conditions by seasonally increasing thermogenic capacity, increasing heterothermy, and displaying highly flexible phenotypes. Other species have evolved to avoid the inhospitable conditions of winter altogether by migrating—again requiring a unique set of physiological adaptations that allow success in this challenging endeavor. In these examples and in many others, the organismal requirements for success share similarities, but the underlying mechanisms, physiological requirements, and selection on those traits can differ significantly, as can their ecological and evolutionary impacts. In recent years, a suite of novel and established tools has become widely available and more accessible, allowing insights into long-standing questions. Genomic tools, new approaches to measure organismal performance, the use of citizen science data, easier access to metabolite assays or hormone detection, to name a few, have spurred rapid advances in our understanding of avian physiology. These new tools have been leveraged to investigate important questions regarding avian responses to our rapidly changing climate in an attempt to understand species resilience and limits. 

Synopsis Many bird species fly at high altitudes for short periods and/or shift seasonally in altitude during migration, but little is known about the physiology of these behaviors. Transient high-altitude flight, or short-term flight at extreme altitudes, is a strategy used by lowland-native birds, often in the absence of topographic barriers. Altitudinal migration, or seasonal roundtrip movement in altitude between the breeding and non-breeding seasons, is a form of migration that occurs as a regular part of the annual cycle and results in periods of seasonal residency at high altitudes. Despite their nuanced differences, these two behaviors share a common challenge: exposure to reduced oxygen environments during at least part of the migratory journey. In this perspective piece, we compare what is known about the physiology of oxygen transport during transient high-altitude flight and altitudinal migration by highlighting case studies and recent conceptual advances from work on captive and wild birds. We aim to open avenues for integrative research on the ecology, evolution, and physiology of high-flying and mountain-climbing birds. 

Synopsis Corticosterone, the main glucocorticoid in birds, is a major mediator of the incredible physiological feat of migration. Corticosterone plays important roles in migration, from preparation to in-flight energy mobilization to refueling, and corticosterone levels often show distinct elevations or depressions during certain stages of the migratory process. Here, we ask whether corticosterone's role in migration shapes its modulation during other life-history stages, as is the case with some other phenotypically flexible traits involved in migration. Specifically, we use a global dataset of corticosterone measures to test whether birds’ migratory status (migrant versus resident) predicts corticosterone levels during breeding. Our results indicate that migratory status predicts neither baseline nor stress-induced corticosterone levels in breeding birds; despite corticosterone’s role in migration, we find no evidence that migratory corticosterone phenotypes carry over to breeding. We encourage future studies to continue to explore corticosterone in migrants versus residents across the annual cycle. Additionally, future efforts should aim to disentangle the possible effects of environmental conditions and migratory status on corticosterone phenotypes; potentially fruitful avenues include focusing on regions where migrants and residents overlap during breeding. Overall, insights from work in this area could demonstrate whether migration shapes traits during other important life stages, identify tradeoffs or limitations associated with the migratory lifestyle, and ultimately shed light on the evolution of flexible traits and migration. 

Synopsis Avian migration is among the most energetically demanding feats observed in animals. Studies evaluating the physiological underpinnings of migration have repeatedly shown that migratory birds display numerous adaptations that ultimately supply the flight muscle mitochondria with abundant fuel and oxygen during long-distance flights. To make use of this high input, the organs and mitochondria of migrants are predicted to display several traits that maximize their capacity to produce adenosine triphosphate (ATP). This review aims to introduce readers to several mechanisms by which organs and mitochondria can alter their capacity for oxidative phosphorylation and ATP production. The role of organ size, mitochondrial volume, substrate, and oxygen delivery to the electron transport system are discussed. A central theme of this review is the role of changes in electron chain complex activity, mitochondrial morphology and dynamics, and supercomplexes in allowing avian migrants and other taxa to alter the performance of the electron transport system with predictable shifts in demand. It is my hope that this review will serve as a springboard for future studies exploring the mechanisms that alter bioenergetic capacity across animal species. 

Synopsis Projected rates of climate change over the next century are expected to force species to shift ranges, adapt, or acclimate to evade extinction. Predicting which of these scenarios may be most likely is a central challenge for conserving biodiversity in the immediate future. Modeling frameworks that take advantage of intraspecific variation across environmental gradients can be particularly important for meeting this challenge. While these space-for-time approaches are essential for climatic and genomic modeling approaches, mechanistic models that incorporate ecological physiology data into assessing species vulnerabilities rarely include intraspecific variation. A major reason for this gap is the general lack of empirical data on intraspecific geographic variation in avian physiological traits. In this review, we outline the evidence for and processes shaping geographic variation in avian traits. We use the example of evaporative water loss to underscore the lack of research on geographic variation, even in traits central to cooling costs in birds. We next demonstrate how shifting the focus of avian physiological research to intraspecific variation can facilitate greater integration with emerging genomics approaches. Finally, we outline important next steps for an integrative approach to advance understanding of avian physiological adaptation within species. Addressing the knowledge gaps outlined in this review will contribute to an improved predictive framework that synthesizes environmental, morphological, physiological, and genomic data to assess species specific vulnerabilities to a warming planet. 

Synopsis Birds exhibit a variety of migration strategies. Because sustained flapping flight requires the production of elevated levels of energy compared to typical daily activities, migratory birds are well-documented to have several physiological adaptations to support the energy demands of migration. However, even though mitochondria are the source of ATP that powers flight, the respiratory performance of the mitochondria is almost unstudied in the context of migration. We hypothesized that migratory species would have higher mitochondrial respiratory performance during migration compared to species that do not migrate. To test this hypothesis, we compared variables related to mitochondrial respiratory function between two confamilial bird species—the migratory Gray Catbird (Dumetella carolinensis) and the non-migratory Northern Mockingbird (Mimus polyglottos). Birds were captured at the same location along the Alabama Gulf Coast, where we assumed that Gray Catbirds were migrants and where resident Northern Mockingbirds live year-round. We found a trend in citrate synthase activity, which suggests that Gray Catbirds have a greater mitochondrial volume in their pectoralis muscle, but we observed no other differences in mitochondrial respiration or complex enzymatic activities between individuals from the migrant vs. the non-migrant species. However, when we assessed the catbirds included in our study using well-established indicators of migratory physiology, birds fell into two groups: a group with physiological parameters indicating a physiology of birds engaged in migration and a group with the physiology of birds not migrating. Thus, our comparison included catbirds that appeared to be outside of migratory condition. When we compared the mitochondrial performance of these three groups, we found that the mitochondrial respiratory capacity of migrating catbirds was very similar to that of Northern Mockingbirds, while the catbirds judged to be not migrating were lowest. One explanation for these observations is these species display very different daily flight behaviors. While the mockingbirds we sampled were not breeding nor migrating, they are highly active birds, living in the open and engaging in flapping flights throughout each day. In contrast, Gray Catbirds live in shrubs and fly infrequently when not migrating. Such differences in baseline energy needs likely confounded our attempt to study adaptations to migration. 

Synopsis Migration is an important life-history strategy that is adopted by a significant proportion of bird species from temperate areas. Birds initiate migration after accumulating considerable energy reserves, primarily in the form of fat and muscle. Sustained exercise, such as during the crossing of ecological barriers, leads to the depletion of energy reservesand increased physiological stress. Stopover sites, where birds rest and restore energy, play a fundamental role in mitigating these challenges. The duration of resting at stopover sites is influenced by environmental and physiological conditions upon arrival, and the amount of body fat reserves plays an important role. While sleep is recognized as essential for all organisms, its importance is accentuated during migration, where energy management becomes a survival constraint. Previous research indicated that individuals with larger fat reserves tend to sleep less and favor an untucked sleep posture, influencing energy recovery and anti-predatory vigilance. We explored the relationship between sleep behavior and posture, metabolic state, and energy conservation strategies during migration in the common whitethroat (Curruca communis). We were able to confirm that sleeping in a tucked position results in metabolic energy savings, at the cost of reduced vigilance. However, whitethroats did not show alterations of their sleep patterns as a response to the amount of stored reserves. This suggests that they may not be taking full advantage of the metabolic gains of sleeping in a tucked posture, at least at this stage of their migratory journey. We suggest that, to achieve optimal fuel accumulation and maximize stopover efficiency, whitethroats prioritize increased foraging over modulating their sleep patterns. 

Synopsis Homeothermic endotherms defend their body temperature in cold environments using a number of behavioral and physiological mechanisms. Maintaining a stable body temperature primarily requires heat production through shivering or non-shivering thermogenesis (NST). Although the use of NST is well established in mammalian systems, the mechanisms and extent to which NST is used in birds are poorly understood. In mammals, one well-characterized mechanism of NST is through uncoupling of Ca2+ transport from ATP hydrolysis by sarco/endoplasmic reticulum ATPase (SERCA) in the skeletal muscle, which generates heat and may contribute to Ca2+ signaling for fatigue resistance and mitochondrial biogenesis. Two small proteins—sarcolipin (SLN) and phospholamban (PLN)—are known to regulate SERCA in mammals, but recent work shows inconsistent responses of SLN to cold acclimation in birds. In this study, we measured SERCA uncoupling in the pectoralis flight muscle of control (18°C) and cold-acclimated (−8°C) dark-eyed juncos (Junco hyemalis) that exhibited suppressed SLN transcription in the cold. We measured SERCA activity and Ca2+ uptake rates for the first time in cold-acclimated birds and found greater SERCA uncoupling in the muscle of juncos in the cold. However, SERCA uncoupling was not related to SLN or PLN transcription or measures of mitochondrial biogenesis. Nonetheless, SERCA uncoupling reduced an individual’s risk of hypothermia in the cold. Therefore, while SERCA uncoupling in the cold could be indicative of NST, it does not appear to be mediated by known regulatory proteins in these birds. These results prompt interesting questions about the significance of SLN and PLN in birds and the role of SERCA uncoupling in response to environmental conditions. 

Synopsis Temperate winters can impose severe conditions on songbirds that threaten survival, including shorter days and often lower temperatures and food availability. One well-studied mechanism by which songbirds cope with such conditions is seasonal acclimatization of thermal metabolic traits, with strong evidence for both preparative and responsive changes in thermogenic capacity (i.e., the ability to generate heat) to low winter temperatures. However, a bird’s ability to cope with seasonal extremes or unpredictable events is likely dependent on a combination of behavioral and physiological traits that function to maintain allostatic balance. The ability to cope with reduced food availability may be an important component of organismal response to temperate winters in songbirds. Here, we compare responses to experimentally reduced food availability at different times of year in captive red crossbills (Loxia curvirostra) and pine siskins (Spinus pinus)—two species that cope with variable food resources and live in cold places—to investigate seasonal changes in the organismal response to food availability. Further, red crossbills are known to use social information to improve responses to reduced food availability, so we also examine whether the use of social information in this context varies seasonally in this species. We find that pine siskins and red crossbills lose less body mass during time-restricted feedings in late winter compared to summer, and that red crossbills further benefit from social information gathered from observing other food-restricted red crossbills in both seasons. Observed changes in body mass were only partially explained by seasonal differences in food intake. Our results demonstrate seasonal acclimation to food stress and social information use across seasons in a controlled captive environment and highlight the importance of considering diverse physiological systems (e.g., thermogenic, metabolic, digestive, etc.) to understand organismal responses to environmental challenges.