It pays to follow the leader: Metabolic cost of flight is lower for trailing birds in small groups.

Many bird species commonly aggregate in flocks for reasons ranging from predator defense to navigation. Available evidence suggests that certain types of flocks-the V and echelon formations of large birds-may provide a benefit that reduces the aerodynamic cost of flight, whereas cluster flocks typical of smaller birds may increase flight costs. However, metabolic flight costs have not been directly measured in any of these group flight contexts [Zhang and Lauder, J. Exp. Biol. 226, jeb245617 (2023)]. Here, we measured the energetic benefits of flight in small groups of two or three birds and the requirements for realizing those benefits, using metabolic energy expenditure and flight position measurements from European Starlings flying in a wind tunnel. The starlings continuously varied their relative position during flights but adopted a V formation motif on average, with a modal spanwise and streamwise spacing of [0.81, 0.91] wingspans. As measured via CO2 production, flight costs for follower birds were significantly reduced compared to their individual solo flight benchmarks. However, followers with more positional variability with respect to leaders did less well, even increasing their costs above solo flight. Thus, we directly demonstrate energetic costs and benefits for group flight followers in an experimental context amenable to further investigation of the underlying aerodynamics, wake interactions, and bird characteristics that produce these metabolic effects.

Long-duration wind tunnel flights reveal exponential declines in protein catabolism over time in short- and long-distance migratory warblers.

During migration, long-distance migratory songbirds may fly nonstop for days, whereas shorter-distance migrants complete flights of 6 to 10 h. Fat is the primary fuel source, but protein is also assumed to provide a low, consistent amount of energy for flight. However, little is known about how the use of these fuel sources differs among bird species and in response to flight duration. Current models predict that birds can fly until fat stores are exhausted, with little consideration of protein's limits on flight range or duration. We captured two related migratory species-ultra long-distance blackpoll warblers (Setophaga striata) and short-distance yellow-rumped warblers (Setophaga coronata)-during fall migration and flew them in a wind tunnel to examine differences in energy expenditure, overall fuel use, and fuel mixture. We measured fat and fat-free body mass before and after flight using quantitative magnetic resonance and calculated energy expenditure from body composition changes and doubly labeled water. Three blackpolls flew voluntarily for up to 28 h-the longest wind tunnel flight to date-and ended flights with substantial fat reserves but concave flight muscle, indicating that protein loss, rather than fat, may actually limit flight duration. Interestingly, while blackpolls had significantly lower mass-specific metabolic power in flight than that of yellow-rumped warblers and fuel use was remarkably similar in both species, with consistent fat use but exceptionally high rates of protein loss at the start of flight that declined exponentially over time. This suggests that protein may be a critical, dynamic, and often overlooked fuel for long-distance migratory birds.

Water restriction increases oxidation of endogenous amino acids in house sparrows (Passer domesticus).

Animals can cope with dehydration in a myriad of ways, both behaviorally and physiologically. The oxidation of protein produces more metabolic water per kilojoule than that of fat or carbohydrate, and it is well established that birds increase protein catabolism in response to high rates of water loss. However, the fate of amino acids mobilized in response to water restriction has not been explicitly determined. While protein catabolism releases bound water, we hypothesized that water-restricted birds would also oxidize the resulting amino acids, producing additional water as a product of oxidative phosphorylation. To test this, we fed captive house sparrows (Passer domesticus) 13C-labeled leucine for 9 weeks to label endogenous proteins. We conducted weekly trials during which we measured the physiological response to water restriction as changes in lean mass, fat mass, metabolism and the enrichment of 13C in exhaled CO2 (δ13Cbreath). If water-restricted birds catabolized proteins and oxidized the resulting amino acids, we expected to simultaneously observe greater lean mass loss and elevated δ13Cbreath relative to control birds. We found that water-restricted birds catabolized more lean tissue and also had enriched δ13Cbreath in response to water restriction, supporting our hypothesis. δ13Cbreath, however, varied with metabolic rate and the length of the water restriction period, suggesting that birds may spare protein when water balance can be achieved using other physiological strategies.

Sarcolipin relates to fattening, but not sarco/endoplasmic reticulum Ca2+-ATPase uncoupling, in captive migratory gray catbirds.

In order to complete their energetically demanding journeys, migratory birds undergo a suite of physiological changes to prepare for long-duration endurance flight, including hyperphagia, fat deposition, reliance on fat as a fuel source, and flight muscle hypertrophy. In mammalian muscle, SLN is a small regulatory protein which binds to sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) and uncouples Ca2+ transport from ATP hydrolysis, increasing energy consumption, heat production, and cytosolic Ca2+ transients that signal for mitochondrial biogenesis, fatigue resistance and a shift to fatty acid oxidation. Using a photoperiod manipulation of captive gray catbirds (Dumetella carolinensis), we investigated whether SLN may play a role in coordinating the development of the migratory phenotype. In response to long-day photostimulation, catbirds demonstrated migratory restlessness and significant body fat stores, alongside higher SLN transcription while SERCA2 remained constant. SLN transcription was strongly correlated with h-FABP and PGC1α transcription, as well as fat mass. However, SLN was not significantly correlated with HOAD or CD36 transcripts or measurements of SERCA activity, SR membrane Ca2+ leak, Ca2+ uptake rates, pumping efficiency or mitochondrial biogenesis. Therefore, SLN may be involved in the process of storing fat and shifting to fat as a fuel, but the mechanism of its involvement remains unclear.

Springing forward: Migrating songbirds catch up with the start of spring in North America.

In temperate regions, the annual pattern of spring onset can be envisioned as a 'green wave' of emerging vegetation that moves across continents from low to high latitudes, signifying increasing food availability for consumers. Many herbivorous migrants 'surf' such resource waves, timing their movements to exploit peak vegetation resources in early spring. Although less well studied at the individual level, secondary consumers such as insectivorous songbirds can track vegetation phenology during migration as well. We hypothesized that four species of ground-foraging songbirds in eastern North America-two warblers and two thrushes-time their spring migrations to coincide with later phases of vegetation phenology, corresponding to increased arthropod prey, and predicted they would match their migration rate to the green wave but trail behind it rather than surfing its leading edge. We further hypothesized that the rate at which spring onset progresses across the continent influences bird migration rates, such that individuals adjust migration timing within North America to phenological conditions they experience en route. To test our hypotheses, we used a continent-wide automated radio telemetry network to track individual songbirds on spring migration between the U.S. Gulf Coast region and northern locations closer to their breeding grounds. We measured vegetation phenology using two metrics of spring onset, the spring index first leaf date and the normalized difference vegetation index (NDVI), then calculated the rate and timing of spring onset relative to bird detections. All individuals arrived in the southeastern United States well after local spring onset. Counter to our expectations, we found that songbirds exhibited a 'catching up' pattern: Individuals migrated faster than the green wave of spring onset, effectively closing in on the start of spring as they approached breeding areas. While surfing of resource waves is a well-documented migration strategy for herbivorous waterfowl and ungulates, individual songbirds in our study migrated faster than the green wave and increasingly caught up to its leading edge en route. Consequently, songbirds experience a range of vegetation phenophases while migrating through North America, suggesting flexibility in their capacity to exploit variable resources in spring.

En las regiones templadas, el patrón anual de inicio de la primavera puede concebirse como una "ola verde" de vegetación emergente que se desplaza por los continentes desde las latitudes bajas a las altas, lo que significa una mayor disponibilidad de alimento para los consumidores. Muchos herbívoros migratorios "surfean" estas olas de recursos, programando sus movimientos para aprovechar los picos de vegetación a principios de primavera. Aunque menos estudiados a nivel de individuo, los consumidores secundarios, como las aves terrestres insectívoras, también pueden seguir la fenología de la vegetación durante la migración. Hipotetizamos es que cuatro especies de aves terrestres que se alimentan en el suelo en el este de Norteamérica - dos reinitas y dos zorzales - programan sus migraciones primaverales para que coincidan con las fases más tardías de la fenología de la vegetación, que se corresponden con un aumento de artrópodos, y predijimos que sincronizarian su ritmo de migración con la ola verde, pero que irían detrás de ella en lugar de surfear su borde delantero. También hipotetizamos que el ritmo al que avanza la primavera en el continente influye en las tasas de migración de las aves, de modo que los individuos ajustan la fecha de migración dentro de Norteamérica a las condiciones fenológicas que experimentan en ruta. Para comprobar nuestras hipótesis, utilizamos una red automatizada de radiotelemetría a escala continental para seguir individuos en su migración primaveral entre la región de la costa del Golfo de EEUU y las localidades septentrionales más cercanas a sus zonas de cría. Medimos la fenología de la vegetación utilizando dos métricas del inicio de la primavera, el índice de la fecha de la primera hoja primaveral y el índice de vegetación de diferencia normalizada (NDVI), luego calculamos la tasa y el tiempo de la aparaciòn de la primavera relativo a las detecciones de aves. Todos los individuos llegaron al sureste de EEUU bastante después del inicio de la primavera local. Contrario a nuestras expectativas, descubrimos que las aves terrestres mostraron un patrón de Carrera para "ponerse al día": los individuos migraron frente a la ola verde del inicio de la primavera, acercándose efectivamente al inicio de la primavera a medida que llegaban a las zonas de cría. Mientras que el surfing de las olas de recursos es una estrategia migratoria bien documentada para las aves acuáticas herbívoras y los ungulados, los individuos de aves terrestres de nuestro estudio migraron más rápido que la ola verde y alcanzaron cada vez más el borde delantero en ruta. En consecuencia, las aves terrestres experimentan una serie de fases fenológicas de la vegetación mientras migran a través de Norteamérica, lo que sugiere flexibilidad en su capacidad para explotar recursos variables en primavera.

White-throated sparrow (Zonotrichia albicollis) liver and pectoralis flight muscle transcriptomic changes in preparation for migration.

Migratory songbirds undertake challenging journeys to reach their breeding grounds each spring. They accomplish these nonstop flapping feats of endurance through a suite of physiological changes, including the development of substantial fat stores and flight muscle hypertrophy and an increased capacity for fat catabolism. In addition, migratory birds may show large reductions in organ masses during flight, including the flight muscle and liver, which they must rapidly rebuild during their migratory stopover before replenishing their fat stores. However, the molecular basis of this capacity for rapid tissue remodeling and energetic output has not been thoroughly investigated. We performed RNA-sequencing analysis of the liver and pectoralis flight muscle of captive white-throated sparrows in experimentally photostimulated migratory and nonmigratory condition to explore the mechanisms of seasonal change to metabolism and tissue mass regulation that may facilitate these migratory journeys. Based on transcriptional changes, we propose that tissue-specific adjustments in preparation for migration may alleviate the damaging effects of long-duration activity, including a potential increase to the inflammatory response in the muscle. Furthermore, we hypothesize that seasonal hypertrophy balances satellite cell recruitment and apoptosis, while little evidence appeared in the transcriptome to support myostatin-, insulin-like growth factor 1-, and mammalian target of rapamycin-mediated pathways for muscle growth. These findings can encourage more targeted molecular studies on the unique integration of pathways that we find in the development of the migratory endurance phenotype in songbirds.NEW & NOTEWORTHY Migratory songbirds undergo significant physiological changes to accomplish their impressive migratory journeys. However, we have a limited understanding of the regulatory mechanisms underlying these changes. Here, we explore the transcriptomic changes to the flight muscle and liver of white-throated sparrows as they develop the migratory condition. We use these patterns to develop hypotheses about metabolic flexibility and tissue restructuring in preparation for migration.

Migratory disposition alters lean mass dynamics and protein metabolism in migratory white-throated sparrows (Zonotrichia albicollis).

Migratory birds seasonally increase fat stores and the capacity to use fat to fuel long-distance migratory flights. However, lean mass loss also occurs during migratory flights and, if adaptive, should exhibit seasonal changes in the capacity for protein metabolism. We conducted a photoperiod manipulation using captive white-throated sparrows (Zonotrichia albicollis) to investigate seasonal changes in protein metabolism between the nonmigratory "winter" condition and after exposure to a long-day "spring" photoperiod to stimulate the migratory condition. After photostimulation, birds in the migratory condition rapidly increased fat mass and activity of fat catabolism enzymes. Meanwhile, total lean mass did not change, but birds increased the activity of protein catabolism enzymes and lost more water and lean mass during water-restricted metabolic testing. These data suggest that more protein may be catabolized during migratory seasons, corresponding with more water loss. Counter to predictions, birds in the migratory condition also showed an approximately 30-fold increase in muscle expression of sarcolipin, which binds to sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) and uncouples Ca2+ transport from ATP hydrolysis. Our documented changes to protein catabolism enzymes and whole animal lean mass dynamics may indicate that protein breakdown or increased protein turnover is adaptive during migration in songbirds.

The effects of training, acute exercise and dietary fatty acid composition on muscle lipid oxidative capacity in European starlings.

Migratory birds undergo seasonal changes to muscle biochemistry. Nonetheless, it is unclear to what extent these changes are attributable to the exercise of flight itself versus endogenous changes. Using starlings (Sturnus vulgaris) flying in a wind tunnel, we tested the effects of exercise training, a single bout of flight and dietary lipid composition on pectoralis muscle oxidative enzymes and lipid transporters. Starlings were either unexercised or trained over 2 weeks to fly in a wind tunnel and sampled either immediately following a long flight at the end of this training or after 2 days recovery from this flight. Additionally, they were divided into dietary groups that differed in dietary fatty acid composition (high polyunsaturates versus high monounsaturates) and amount of dietary antioxidant. Trained starlings had elevated (19%) carnitine palmitoyl transferase and elevated (11%) hydroxyacyl-CoA dehydrogenase in pectoralis muscle compared with unexercised controls, but training alone had little effect on lipid transporters. Immediately following a long wind-tunnel flight, starling pectoralis had upregulated lipid transporter mRNA (heart-type fatty acid binding protein, H-FABP, 4.7-fold; fatty acid translocase, 1.9-fold; plasma membrane fatty acid binding protein, 1.6-fold), and upregulated H-FABP protein (68%). Dietary fatty acid composition and the amount of dietary antioxidants had no effect on muscle catabolic enzymes or lipid transporter expression. Our results demonstrate that birds undergo rapid upregulation of catabolic capacity that largely becomes available during flight itself, with minor effects due to training. These effects likely combine with endogenous seasonal changes to create the migratory phenotype observed in the wild.

Aminopeptidase-N modulation assists lean mass anabolism during refuelling in the white-throated sparrow.

Songbirds meet the extreme metabolic demands of migration by burning both stored fat and protein. However, catabolizing these endogenous tissues for energy leads to organ atrophy, and reductions in gastrointestinal tissue can be as great as 50% of the pre-flight mass. Remarkably, during stopover refuelling birds quickly regain digestive mass and performance. Aminopeptidase-N (APN) is a brush-border enzyme responsible for late-stage protein digestion and may critically assist tissue reconstruction during the stopover, thus compensating for reduced gut size. We hypothesized that birds recovering from a fast would differentially upregulate APN activity relative to disaccharidases to rapidly process and assimilate dietary protein into lean mass. We fasted 23 wild-caught migratory white-throated sparrows (Zonotrichia albicollis) for 48 h to mimic mass reductions experienced during migratory flight and measured intestinal APN activity before the fast, immediately after the fast, and during recovery at 24 h and 48 h post-fast. Total fat mass, lean mass and basal metabolic rate were measured daily. We show that fasted birds maintain APN activity through the fast, despite a 30% reduction in intestine mass, but during refuelling, APN activity increases nearly twofold over pre-fasted individuals. This suggests that dynamically regulating APN may be necessary for rapid protein reconstruction during the stopover.

Thermoregulation in desert birds: scaling and phylogenetic variation in heat tolerance and evaporative cooling.

Evaporative heat dissipation is a key aspect of avian thermoregulation in hot environments. We quantified variation in avian thermoregulatory performance at high air temperatures (Ta) using published data on body temperature (Tb), evaporative water loss (EWL) and resting metabolic rate (RMR) measured under standardized conditions of very low humidity in 56 arid-zone species. Maximum Tb during acute heat exposure varied from 42.5±1.3°C in caprimulgids to 44.5±0.5°C in passerines. Among passerines, both maximum Tb and the difference between maximum and normothermic Tb decreased significantly with body mass (Mb). Scaling exponents for minimum thermoneutral EWL and maximum EWL were 0.825 and 0.801, respectively, even though evaporative scope (ratio of maximum to minimum EWL) varied widely among species. Upper critical limits of thermoneutrality (Tuc) varied by >20°C and maximum RMR during acute heat exposure scaled to Mb0.75 in both the overall data set and among passerines. The slope of RMR at Ta>Tuc increased significantly with Mb but was substantially higher among passerines, which rely on panting, compared with columbids, in which cutaneous evaporation predominates. Our analysis supports recent arguments that interspecific within-taxon variation in heat tolerance is functionally linked to evaporative scope and maximum ratios of evaporative heat loss (EHL) to metabolic heat production (MHP). We provide predictive equations for most variables related to avian heat tolerance. Metabolic costs of heat dissipation pathways, rather than capacity to increase EWL above baseline levels, appear to represent the major constraint on the upper limits of avian heat tolerance.

Developing a Stopover-CORT hypothesis: Corticosterone predicts body composition and refueling rate in Gray Catbirds during migratory stopover.

Migratory flight is energetically challenging, requiring alternating phases of fuel catabolism and fuel accumulation, accompanied by dramatic changes in body composition and behavior. Baseline corticosterone (CORT; the primary glucocorticoid in birds) is thought to underlie transitions between fuel catabolism during flight, fuel deposition during stopover, and the initiation of migratory flight. However, studies of CORT on stopover physiology and behavior remain disparate efforts, lacking the cohesion of a general hypothesis. Here we develop a Stopover-CORT hypothesis formalizing the relationships among CORT, body condition, and refueling rate in migratory birds. First we expect body mass to increase with triglycerides (TRIG) as birds refuel. Second, based on a synthesis of previous literature, we predict a U-shaped CORT curve over the course of stopover, postulating that elevated CORT at arrival is reactive, responding to poor body condition, while CORT elevation before departure is preparative, driving changes in behavior and body condition. We tested these predictions in Gray Catbirds (Dumetella carolinensis) following a trans-Gulf flight during spring migration. We found baseline CORT was negatively correlated with body condition and TRIG, corresponding with our predictions for arriving and refueling-but not departing-birds. It is possible catbirds undergo regional habitat translocations rather than complete the entire stopover phase at our study site. We propose the Stopover-CORT hypothesis as a useful predictive framework for future studies of the mechanistic basis of stopover physiology. By studying the regulation of stopover refueling and departure, we may better understand physiological limitations to overall migration rate and improve assessments of habitat quality for refueling birds.

Metabolic reduction after long-duration flight is not related to fat-free mass loss or flight duration in a migratory passerine.

Migratory birds catabolize large quantities of protein during long flights, resulting in dramatic reductions in organ and muscle mass. One of the many hypotheses to explain this phenomenon is that decrease in lean mass is associated with reduced resting metabolism, saving energy after flight during refueling. However, the relationship between lean body mass and resting metabolic rate remains unclear. Furthermore, the coupling of lean mass with resting metabolic rate and with peak metabolic rate before and after long-duration flight have not previously been explored. We flew migratory yellow-rumped warblers (Setophaga coronata) in a wind tunnel under one of two humidity regimes to manipulate the rate of lean mass loss in flight, decoupling flight duration from total lean mass loss. Before and after long-duration flights, we measured resting and peak metabolism, and also measured fat mass and lean body mass using quantitative magnetic resonance. Flight duration ranged from 28 min to 600 min, and birds flying under dehydrating conditions lost more fat-free mass than those flying under humid conditions. After flight, there was a 14% reduction in resting metabolism but no change in peak metabolism. Interestingly, the reduction in resting metabolism was unrelated to flight duration or to change in fat-free body mass, indicating that protein metabolism in flight is unlikely to have evolved as an energy-saving measure to aid stopover refueling, but metabolic reduction itself is likely to be beneficial to migratory birds arriving in novel habitats.

Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration.

Extreme high environmental temperatures produce a variety of consequences for wildlife, including mass die-offs. Heat waves are increasing in frequency, intensity, and extent, and are projected to increase further under climate change. However, the spatial and temporal dynamics of die-off risk are poorly understood. Here, we examine the effects of heat waves on evaporative water loss (EWL) and survival in five desert passerine birds across the southwestern United States using a combination of physiological data, mechanistically informed models, and hourly geospatial temperature data. We ask how rates of EWL vary with temperature across species; how frequently, over what areas, and how rapidly lethal dehydration occurs; how EWL and die-off risk vary with body mass; and how die-off risk is affected by climate warming. We find that smaller-bodied passerines are subject to higher rates of mass-specific EWL than larger-bodied counterparts and thus encounter potentially lethal conditions much more frequently, over shorter daily intervals, and over larger geographic areas. Warming by 4 °C greatly expands the extent, frequency, and intensity of dehydration risk, and introduces new threats for larger passerine birds, particularly those with limited geographic ranges. Our models reveal that increasing air temperatures and heat wave occurrence will potentially have important impacts on the water balance, daily activity, and geographic distribution of arid-zone birds. Impacts may be exacerbated by chronic effects and interactions with other environmental changes. This work underscores the importance of acute risks of high temperatures, particularly for small-bodied species, and suggests conservation of thermal refugia and water sources.

The role of humidity and metabolic status on lean mass catabolism in migratory Swainson's thrushes (Catharus ustulatus).

Migratory birds use protein as a fuel source during flight, but the mechanisms and benefits of protein catabolism during migration are poorly understood. The tissue-specific turnover rate hypothesis proposes that lean mass loss depends solely on the constitutive rate of protein degradation for a given tissue, and is therefore independent of metabolic rate or environmental stimuli. However, it has been demonstrated that environmental stressors such as humidity affect the rate of lean mass catabolism during flight, a finding that seemingly contradicts the tissue-specific turnover rate hypothesis. In order to resolve this, we placed migratory Swainson's thrushes in either high (HEWL) or low (LEWL) evaporative water loss conditions at rest and while undergoing simulated migratory flight at 8 m s-1 in a wind tunnel to test the impact of both environmental stressors and metabolic rate on the rate of protein breakdown. The total quantity and rate of lean mass loss was not different between flight and rest birds, but was affected by humidity condition, with HEWL losing significantly more lean mass. These results show that the rate of protein breakdown in migratory birds is independent of metabolic rate, but it can be augmented in response to environmental stressors.

Avian thermoregulation in the heat: metabolism, evaporative cooling and gular flutter in two small owls.

The thermoregulatory responses of owls to heat stress have been the subject of few studies. Although nocturnality buffers desert-dwelling owls from significant heat stress during activity, roost sites in tree and cactus cavities or in deep shade provide only limited refuge from high environmental temperatures during the day. We measured thermoregulatory responses to acute heat stress in two species of small owls, the elf owl (Micrathene whitneyi) and the western screech-owl (Megascops kennicottii), which occupy the Sonoran Desert of southwestern North America, an area of extreme heat and aridity. We exposed wild-caught birds to progressively increasing air temperatures (Ta) and measured resting metabolic rate (RMR), evaporative water loss (EWL), body temperature (Tb) and heat tolerance limits (HTL; the maximum Ta reached). Comparatively low RMR values were observed in both species, Tb approximated Ta at 40°C and mild hyperthermia occurred as Ta was increased toward the HTL. Elf owls and screech-owls reached HTLs of 48 and 52°C, respectively, and RMR increased to 1.5 and 1.9 times thermoneutral values. Rates of EWL at the HTL allowed for the dissipation of 167-198% of metabolic heat production (MHP). Gular flutter was used as the primary means of evaporative heat dissipation and produced large increases in evaporative heat loss (44-100%), accompanied by only small increases (<5%) in RMR. These small, cavity-nesting owls have thermoregulatory capacities that are intermediate between those of the open-ground nesting nightjars and the passerines that occupy the same ecosystem.

Avian thermoregulation in the heat: phylogenetic variation among avian orders in evaporative cooling capacity and heat tolerance.

Little is known about the phylogenetic variation of avian evaporative cooling efficiency and heat tolerance in hot environments. We quantified thermoregulatory responses to high air temperature (Ta) in ∼100-g representatives of three orders, namely, the African cuckoo (Cuculus gularis, Cuculiformes), lilac-breasted roller (Coracias caudatus, Coraciiformes) and Burchell's starling (Lamprotornis australis, Passeriformes). All three species initiated respiratory mechanisms to increase evaporative heat dissipation when body temperature (Tb) approached 41.5°C in response to increasing Ta, with gular flutter observed in cuckoos and panting in rollers and starlings. Resting metabolic rate and evaporative water loss increased by quantitatively similar magnitudes in all three species, although maximum rates of evaporative water loss were proportionately lower in starlings. Evaporative cooling efficiency [defined as the ratio of evaporative heat loss (EHL) to metabolic heat production (MHP)] generally remained below 2.0 in cuckoos and starlings, but reached a maximum of ∼3.5 in rollers. The high value for rollers reveals a very efficient evaporative cooling mechanism, and is similar to EHL/MHP maxima for similarly sized columbids which very effectively dissipate heat via cutaneous evaporation. This unexpected phylogenetic variation among the orders tested in the physiological mechanisms of heat dissipation is an important step toward determining the evolution of heat tolerance traits in desert birds.

Avian thermoregulation in the heat: evaporative cooling capacity and thermal tolerance in two Australian parrots.

Avian orders differ in their thermoregulatory capabilities and tolerance of high environmental temperatures. Evaporative heat loss, and the primary avenue whereby it occurs, differs amongst taxa. Although Australian parrots (Psittaciformes) have been impacted by mass mortality events associated with extreme weather events (heat waves), their thermoregulatory physiology has not been well characterized. We quantified the upper limits to thermoregulation under extremely hot conditions in two Australian parrots: the mulga parrot (Psephotellus varius; ∼55 g) and the galah (Eolophus roseicapilla; ∼265 g). At air temperatures (Ta) exceeding body temperature (Tb), both species showed increases in Tb to maximum values around 43-44°C, accompanied by rapid increases in resting metabolic rate above clearly defined upper critical limits of thermoneutrality and increases in evaporative water loss to levels equivalent to 700-1000% of baseline rates at thermoneutral Ta Maximum cooling capacity, quantified as the fraction of metabolic heat production dissipated evaporatively, ranged from 1.71 to 1.79, consistent with the known range for parrots, similar to the corresponding range in passerines, and well below the corresponding ranges for columbids and caprimulgids. Heat tolerance limit (the maximum Ta tolerated) ranged from 44 to 55°C, similar to the range reported for passerines, but lower than that reported for columbids and caprimulgids. Our data suggest that heat tolerance in parrots is similar to that in passerines. We argue that understanding how thermoregulatory capacity and heat tolerance vary across avian orders is vital for predicting how climate change and the associated increase in frequency of extreme weather events may impact avian populations in the future.

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.

The performing animal: causes and consequences of body remodeling and metabolic adjustments in red knots facing contrasting thermal environments.

Using red knots (Calidris canutus) as a model, we determined how changes in mass and metabolic activity of organs relate to temperature-induced variation in metabolic performance. In cold-acclimated birds, we expected large muscles and heart as well as improved oxidative capacity and lipid transport, and we predicted that this would explain variation in maximal thermogenic capacity (Msum). We also expected larger digestive and excretory organs in these same birds and predicted that this would explain most of the variation in basal metabolic rate (BMR). Knots kept at 5°C were 20% heavier and maintained 1.5 times more body fat than individuals kept in thermoneutral conditions (25°C). The birds in the cold also had a BMR up to 32% higher and a Msum 16% higher than birds at 25°C. Organs were larger in the cold, with muscles and heart being 9-20% heavier and digestive and excretory organs being 21-36% larger than at thermoneutrality. Rather than the predicted digestive and excretory organs, the cold-induced increase in BMR correlated with changes in mass of the heart, pectoralis, and carcass. Msum varied positively with the mass of the pectoralis, supracoracoideus, and heart, highlighting the importance of muscles and cardiac function in cold endurance. Cold-acclimated knots also expressed upregulated capacity for lipid transport across mitochondrial membranes [carnitine palmitoyl transferase (CPT)] in their pectoralis and leg muscles, higher lipid catabolism capacity in their pectoralis muscles [ß-hydroxyacyl CoA-dehydrogenase (HOAD)], and elevated oxidative capacity in their liver and kidney (citrate synthase). These adjustments may have contributed to BMR through changes in metabolic intensity. Positive relationships among Msum, CPT, and HOAD in the heart also suggest indirect constraints on thermogenic capacity through limited cardiac capacity.

Avian thermoregulation in the heat: evaporative cooling capacity of arid-zone Caprimulgiformes from two continents.

Birds in the order Caprimulgiformes (nightjars and allies) have a remarkable capacity for thermoregulation over a wide range of environmental temperatures, exhibiting pronounced heterothermy in cool conditions and extreme heat tolerance at high environmental temperatures. We measured thermoregulatory responses to acute heat stress in three species of Caprimulgiformes that nest in areas of extreme heat and aridity, the common poorwill (Phalaenoptilus nuttallii: Caprimulgidae) and lesser nighthawk (Chordeiles acutipennis: Caprimulgidae) in the Sonoran Desert of Arizona, and the Australian owlet-nightjar (Aegotheles cristatus: Aegothelidae) in the mallee woodlands of South Australia. We exposed wild-caught birds to progressively increasing air temperatures (Ta) and measured resting metabolic rate (RMR), evaporative water loss (EWL), body temperature (Tb) and heat tolerance limit (HTL; the maximum Ta reached). Comparatively low RMR values were observed in all species (0.35, 0.36 and 0.40 W for the poorwill, nighthawk and owlet-nightjar, respectively), with Tb approximating Ta at 40°C and mild hyperthermia occurring as Ta reached the HTL. Nighthawks and poorwills reached HTLs of 60 and 62°C, respectively, whereas the owlet-nightjar had a HTL of 52°C. RMR increased gradually above minima at Ta of 42, 42 and 35°C, and reached 1.7, 1.9 and 2.0 times minimum resting values at HTLs in the poorwill, nighthawk and owlet-nightjar, respectively. EWL increased rapidly and linearly as Ta exceeded Tb and resulted in maximum rates of evaporative heat dissipation equivalent to 237-424% of metabolic heat production. Bouts of gular flutter resulted in large transient increases in evaporative heat loss (50-123%) accompanied by only small increments in RMR (<5%). The cavity-nesting/roosting owlet-nightjar had a lower HTL and less efficient evaporative cooling compared with the species that nest and/or roost on open desert surfaces. The high efficiency of gular flutter for evaporative cooling, combined with mild hyperthermia, provides the physiological basis for defending Tb well below Ta in extreme heat and is comparable to the efficient cooling observed in arid-zone columbids in which cutaneous EWL is the predominant cooling pathway.