Environmental Physiology of Flight in Migratory Birds

Migratory birds complete amazing journeys between their breeding and wintering grounds. Each journey comprises a series of flights that last hours to days, followed by stopovers where fuel stores are replenished. Despite the long flights undertaken by migratory birds, where respiratory water losses are high for extended periods of time, birds are not dehydrated after flight. My studies demonstrate that birds maintain hydration by modulating rates of endogenous water production in response to rates of water loss. In resting, water restricted house sparrows (Passer domesticus) I used quantitative magnetic resonance body composition analysis (QMR) and hygrometry to demonstrate that stressed resting birds increase the rate of lean mass (protein) catabolism to liberate water and maintain osmotic homeostasis. I then flew Swainson’s thrushes (Catharus ustulatus) in a climatic wind tunnel under high- and low-humidity conditions for up to 5 hours. Flight under dry conditions increased the rate of lean mass loss, endogenous water production and plasma uric acid concentrations. This demonstrated that atmospheric humidity influences fuel composition in flight and suggest that protein deposition and catabolism during migration are a metabolic strategy to maintain osmotic homeostasis during flight. Next, I investigated the metabolic response to flight in the American robin (Turdus migratorius). These birds have high rates of endogenous water production early in flight due to a high contribution of carbohydrate and protein to energy during the transition to fat oxidation, and do not require additional protein catabolism to maintain water balance. Migratory birds may reduce excretory water losses to avoid dehydration in flight. I investigated kidney function in fed, rested and flown Swainson’s thrushes and found no decrease in glomerular filtration rate during flight, however they rely on increased water reabsorption to reduce excretory water losses in flight and at rest. Finally, the effect of diet on mitochondrial metabolism was investigated. I demonstrated that the performance increases often attributed to high dietary polyunsaturated fatty acids are likely due to reduced rates of production of reactive oxygen species by mitochondria. Together, these studies advance our knowledge of the metabolic response to the environment in the context of bird migration

Mobilization of mercury from lean tissues during simulated migratory fasting in a model songbird

The pollutant methylmercury accumulates within lean tissues of birds and other animals. Migrating birds catabolize substantial amounts of lean tissue during flight which may mobilize methylmercury and increase circulating levels of this neurotoxin. As a model for a migrating songbird, we fasted zebra finches (Taeniopygia guttata) that had been dosed with 0.0, 0.1, and 0.6 parts per million (ppm) dietary methylmercury and measured changes in blood total mercury concentrations (THg) in relation to reductions in lean mass. Birds lost 6-16% of their lean mass during the fast, and THg increased an average of 12% and 11% in the 0.1 and 0.6 ppm treatments, respectively. Trace amounts of THg in the 0.0 ppm control group also increased as a result of fasting, but remained extremely low. THg increased 0.4 ppm for each gram of lean mass catabolized in the higher dose birds. Our findings indicate that methylmercury is mobilized from lean tissues during protein catabolism and results in acute increases in circulating concentrations. This is a previously undocumented potential threat to wild migratory birds, which may experience greater surges in circulating methylmercury than demonstrated here as a result of their greater reductions in lean mass

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 maximumRMR during acute heat exposure scaled toMb 0.75 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, comparedwith 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.The National Research Foundation and the National Science Foundation.http://jeb.biologists.orgam2022Zoology and Entomolog

Constitutive immune function in European starlings, \u3cem\u3eSturnus vulgaris\u3c/em\u3e, is decreased immediately after an endurance flight in a wind tunnel

Life-history theory predicts that animals face a trade-off in energy allocation between performing strenuous exercise, such as migratory flight, and mounting an immune response. We experimentally tested this prediction by studying immune function in European starlings, Sturnus vulgaris, flown in a wind tunnel. Specifically, we predicted that constitutive immune function decreases in response to training and, additionally, in response to immediate exercise. We compared constitutive immune function among three groups: (1) ‘untrained’ birds that were kept in cages and were not flown; (2) ‘trained’ birds that received flight training over a 15 day period and performed a 1-4 h continuous flight, after which they rested for 48 h before being sampled; and (3) ‘post-flight’ birds that differed from the ‘trained’ group only in being sampled immediately after the final flight. A bird in our trained group represents an individual during migration that has been resting between migratory flights for at least 2 days. A bird in our post-flight group represents an individual that has just completed a migratory flight and has not yet had time to recover. Three of our four indicators (haptoglobin, agglutination and lysis) showed the predicted decrease in immune function in the post-flight group, and two indicators (haptoglobin, agglutination) showed the predicted decreasing trend from the untrained to trained to post-flight group. Haptoglobin levels were negatively correlated with flight duration. No effect of training or flight was detected on leukocyte profiles. Our results suggest that in European starlings, constitutive immune function is decreased more as a result of immediate exercise than of exercise training. Because of the recent emergence of avian-borne diseases, understanding the trade-offs and challenges faced by long-distance migrants has gained a new level of relevance and urgency

Migration- and exercise-induced changes to flight muscle size in migratory birds and association with \u3cem\u3eIGF1\u3c/em\u3e and \u3cem\u3emyostatin\u3c/em\u3e mRNA expression

Seasonal adjustments to muscle size in migratory birds may result from preparatory physiological changes or responses to changed workloads. The mechanisms controlling these changes in size are poorly understood. We investigated some potential mediators of flight muscle size (myostatin and insulin-like growth factor, IGF1) in pectoralis muscles of wild wintering or migrating white-throated sparrows (Zonotrichia albicollis), captive white-throated sparrows that were photoperiod manipulated to be in a `wintering\u27 or `migratory\u27 (Zugunruhe) state, and captive European starlings (Sturnus vulgaris) that were either exercised for 2 weeks in a wind tunnel or untrained. Flight muscle size increased in photo-stimulated `migrants\u27 and in exercised starlings. Acute exercise but not long-term training caused increased expression of IGF1, but neither caused a change in expression of myostatin or its metalloprotease activator TLL1. Photo-stimulated `migrant\u27 sparrows demonstrated increased expression of both myostatin and IGF1, but wild sparrows exhibited no significant seasonal changes in expression of either myostatin or IGF1. Additionally, in both study species we describe several splice variants of myostatin that are shared with distantly related bird species. We demonstrate that their expression patterns are not different from those of the typical myostatin, suggesting that they have no functional importance and may be mistakes of the splicing machinery. We conclude that IGF1 is likely to be an important mediator of muscle phenotypic flexibility during acute exercise and during endogenous, seasonal preparation for migration. The role of myostatin is less clear, but its paradoxical increase in photo-stimulated `migrants\u27 may indicate a role in seasonal adjustments of protein turnover

Nonlinear Decline-Rate Dependence and Intrinsic Variation of Type Ia Supernova Luminosities

Published B and V fluxes from nearby Type Ia supernovae are fitted to light-curve templates with 4-6 adjustable parameters. Separately, B magnitudes from the same sample are fitted to a linear dependence on B-V color within a post-maximum time window prescribed by the CMAGIC method. These fits yield two independent SN magnitude estimates B_max and B_BV. Their difference varies systematically with decline rate Delta m_15 in a form that is compatible with a bilinear but not a linear dependence; a nonlinear form likely describes the decline-rate dependence of B_max itself. A Hubble fit to the average of B_max and B_BV requires a systematic correction for observed B-V color that can be described by a linear coefficient R = 2.59 +- 0.24, well below the coefficient R_B ~ 4.1 commonly used to characterize the effects of Milky Way dust. At 99.9% confidence the data reject a simple model in which no color correction is required for SNe that are clustered at the blue end of their observed color distribution. After systematic corrections are performed, B_max and B_BV exhibit mutual rms intrinsic variation equal to 0.074 +- 0.019 mag, of which at least an equal share likely belongs to B_BV. SN magnitudes measured using maximum-luminosity or CMAGIC methods show comparable rms deviations of order ~ 0.14 mag from the Hubble line. The same fit also establishes a 95% confidence upper limit of 486 km/s on the rms peculiar velocity of nearby SNe relative to the Hubble flow.Comment: 21 pages, 11 figures, 10 tables, to appear in The Astrophysical Journal, uses emulateapj_051214.cl

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

Triple Oxygen Isotope Measurements (Δ\u27\u3csup\u3e17\u3c/sup\u3eO) of Body Water Reflect Water Intake, Metabolism, and δ\u3csup\u3e18\u3c/sup\u3eO of Ingested Water in Passerines

Understanding physiological traits and ecological conditions that influence a species reliance on metabolic water is critical to creating accurate physiological models that can assess their ability to adapt to environmental perturbations (e.g., drought) that impact water availability. However, relatively few studies have examined variation in the sources of water animals use to maintain water balance, and even fewer have focused on the role of metabolic water. A key reason is methodological limitations. Here, we applied a new method that measures the triple oxygen isotopic composition of a single blood sample to estimate the contribution of metabolic water to the body water pool of three passerine species. This approach relies on Δ\u2717O, defined as the residual from the tight linear correlation that naturally exists between δ17O and δ18O values. Importantly, Δ\u2717O is relatively insensitive to key fractionation processes, such as Rayleigh distillation in the water cycle that have hindered previous isotope-based assessments of animal water balance. We evaluated the effects of changes in metabolic rate and water intake on Δ\u2717O values of captive rufous-collared sparrows (Zonotrichia capensis) and two invertivorous passerine species in the genus Cinclodes from the field. As predicted, colder acclimation temperatures induced increases in metabolic rate, decreases in water intake, and increases in the contribution of metabolic water to the body water pool of Z. capensis, causing a consistent change in Δ\u2717O. Measurement of Δ\u2717O also provides an estimate of the δ18O composition of ingested pre-formed (drinking/food) water. Estimated δ18O values of drinking/food water for captive Z. capensis were ~ −11‰, which is consistent with that of tap water in Santiago, Chile. In contrast, δ18O values of drinking/food water ingested by wild-caught Cinclodeswere similar to that of seawater, which is consistent with their reliance on marine resources. Our results confirm the utility of this method for quantifying the relative contribution of metabolic versus pre-formed drinking/food water to the body water pool in birds

The impact of humidity on evaporative cooling in small desert birds exposed to high air temperatures

Environmental temperatures that exceed body temperature (Tb) force endothermic animals to rely solely on evaporative cooling to dissipate heat. However, evaporative heat dissipation can be drastically reduced by environmental humidity, imposing a thermoregulatory challenge. The goal of this study was to investigate the effects of humidity on the thermoregulation of desert birds and to compare the sensitivity of cutaneous and respiratory evaporation to reduced vapor density gradients. Rates of evaporative water loss, metabolic rate, and Tb were measured in birds exposed to humidities ranging from ∼2 to 30 g H2O m23 (0%–100% relative humidity at 307C) at air temperatures between 447 and 567C. In sociable weavers, a species that dissipates heat primarily through panting, rates of evaporative water loss were inhibited by as much as 36% by high humidity at 487C, and these birds showed a high degree of hyperthermia. At lower temperatures (407–447C), evaporative water loss was largely unaffected by humidity in this species. In Namaqua doves, which primarily use cutaneous evaporation, increasing humidity reduced rates of evaporative water loss, but overall rates of water loss were lower than those observed in sociable weavers. Our data suggest that cutaneous evaporation is more efficient than panting, requiring less water to maintain Tb at a given temperature, but panting appears less sensitive to humidity over the air temperature range investigated here.DST/National Research Foundation Centre of Excellencehttp://www.journals.uchicago.edutoc/pbz/tm201

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 Wfor the poorwill, nighthawk and owletnightjar, 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 owletnightjar, 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 owletnightjar 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.The National Science Foundation under IOS-1122228 to B.O.W.http://jeb.biologists.org2018-10-01am2018Zoology and Entomolog