Bar-headed geese (Anser indicus) fly at high altitudes during their migration across the Himalayas and Tibetan plateau. However, we know relatively little about whether rearing at high altitude (i.e. phenotypic plasticity) facilitates this impressive feat because most of what is known about their physiology comes from studies performed at sea level. To provide this information, a comprehensive analysis of metabolic, cardiovascular and ventilatory responses to progressive decreases in the equivalent fractional composition of inspired oxygen (FI O2 : 0.21, 0.12, 0.09, 0.07 and 0.05) was made on bar-headed geese reared at either high altitude (3200 m) or low altitude (0 m) and on barnacle geese (Branta leucopsis), a low-altitude migrating species, reared at low altitude (0 m). Bar-headed geese reared at high altitude exhibited lower metabolic rates and a modestly increased hypoxic ventilatory response compared with low-altitudereared bar-headed geese. Although the in vivo oxygen equilibrium curves and blood-oxygen carrying capacity did not differ between the two bar-headed goose study groups, the blood-oxygen carrying capacity was higher than that of barnacle geese. Resting cardiac output also did not differ between groups and increased at least twofold during progressive hypoxia, initially as a result of increases in stroke volume. However, cardiac output increased at a higher FI O2 threshold in bar-headed geese raised at high altitude. Thus, bar-headed geese reared at high altitude exhibited a reduced oxygen demand at rest and a modest but significant increase in oxygen uptake and delivery during progressive hypoxia compared with barheaded geese reared at low altitude.

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Many high-altitude vertebrates have evolved increased capacities in their oxygen transport cascade (ventilation, pulmonary diffusion, circulation and tissue diffusion), enhancing oxygen transfer from the atmosphere to mitochondria. However, the extent of interspecies variation in the control processes that dictate hypoxia responses remains largely unknown. We compared the metabolic, cardiovascular and respiratory responses to progressive decreases in inspired oxygen levels of bar-headed geese (), birds that biannually migrate across the Himalayan mountains, with those of Andean geese () and crested ducks (), lifelong residents of the high Andes. We show that Andean geese and crested ducks have evolved fundamentally different mechanisms for maintaining oxygen supply during low oxygen (hypoxia) from those of bar-headed geese. Bar-headed geese respond to hypoxia with robust increases in ventilation and heart rate, whereas Andean species increase lung oxygen extraction and cardiac stroke volume. We propose that transient high-altitude performance has favoured the evolution of robust convective oxygen transport recruitment in hypoxia, whereas life-long high-altitude residency has favoured the evolution of structural enhancements to the lungs and heart that increase lung diffusion and stroke volume.

SUMMARYAnoxic survival requires the matching of cardiac ATP supply (i.e. maximum glycolytic potential, MGP) and demand (i.e. cardiac power output, PO). We examined the idea that the previously observed in vivo downregulation of cardiac function during exposure to severe hypoxia in tilapia (Oreochromis hybrid) represents a physiological strategy to reduce routine PO to within the heartʼs MGP. The MGP of the ectothermic vertebrate heart has previously been suggested to be ~70nmol ATPs -1 NaCN) on cardiac performance in severe hypoxia were also examined. Under normoxic conditions, cardiac performance and myocardial oxygen consumption rate were comparable to those of other teleosts. The tilapia heart maintained a routine normoxic cardiac output (Q) and PO under all hypoxic conditions, a result that contrasts with the hypoxic cardiac downregulation previously observed in vivo under less severe conditions. Thus, we conclude that the in vivo downregulation of routine cardiac performance in hypoxia is not needed in tilapia to balance cardiac energy supply and demand. Indeed, the MGP of the tilapia heart proved to be quite exceptional. Measurements of myocardial lactate efflux during severe hypoxia were used to calculate the MGP of the tilapia heart. The MGP was estimated to be 172nmol ATPs , which is only 30% lower than the PO max observed with normoxia. Even with this MGP, the additional challenge of acidosis during severe hypoxia decreased maximum ATP turnover rate and PO max by 30% compared with severe hypoxia alone, suggesting that there are probably direct effects of acidosis on cardiac contractility. We conclude that the high maximum glycolytic ATP turnover rate and levels of PO, which exceed those measured in other ectothermic vertebrate hearts, probably convey a previously unreported anoxia tolerance of the tilapia heart, but a tolerance that may be tempered in vivo by the accumulation of acidotic waste during anoxia.

The metabolic cost of breathing at rest has never been successfully measured in birds, but has been hypothesized to be higher than in mammals of a similar size because of the rocking motion of the avian sternum being encumbered by the pectoral flight muscles. To measure the cost and work of breathing, and to investigate whether species resident at high altitude exhibit morphological or mechanical changes that alter the work of breathing, we studied 11 species of waterfowl: five from high altitudes (>3000 m) in Peru, and six from low altitudes in Oregon, USA. Birds were anesthetized and mechanically ventilated in sternal recumbency with known tidal volumes and breathing frequencies. The work done by the ventilator was measured, and these values were applied to the combinations of tidal volumes and breathing frequencies used by the birds to breathe at rest. We found the respiratory system of high-altitude species to be of a similar size, but consistently more compliant than that of lowaltitude sister taxa, although this did not translate to a significantly reduced work of breathing. The metabolic cost of breathing was estimated to be between 1 and 3% of basal metabolic rate, as low or lower than estimates for other groups of tetrapods.

High altitude is physiologically challenging for vertebrate life for many reasons, including hypoxia (low environmental oxygen); yet, many birds thrive at altitude. Compared with mammals, birds have additional enhancements to their oxygen transport cascade, the conceptual series of steps responsible for acquiring oxygen from the environment and transporting it to the mitochondria. These adaptations have allowed them to inhabit a number of high-altitude regions. Waterfowl are a taxon prolific at altitude. This minireview explores the physiological responses of high-altitude waterfowl (geese and ducks), comparing the strategies of lifelong high-altitude residents to those of transient high-altitude performers, providing insight into how birds champion high-altitude life. In particular, this review highlights and contrasts the physiological hypoxia responses of bar-headed geese (), birds that migrate biannually through the Himalayas (4,500-6,500 m), and Andean geese (), lifelong residents of the Andes (4,000-5,500 m). These two species exhibit markedly different ventilatory and cardiovascular strategies for coping with hypoxia: bar-headed geese robustly increase convective oxygen transport elements (i.e., heart rate and total ventilation) whereas Andean geese rely predominantly on enhancements that are likely morphological in origin (i.e., increases in lung oxygen diffusion and cardiac stroke volume). The minireview compares the short- and long-term cardiovascular and ventilatory trade-offs of these different physiological strategies and offers hypotheses surrounding their origins. It also draws parallels to high-altitude human physiology and research, and identifies a number of areas of further research. The field of high-altitude avian physiology offers a unique and broadly applicable insight into physiological enhancements in hypoxia.

The ability to maintain stable cardiac function during environmental hypoxia exposure is crucial for hypoxia tolerance in animals and depends upon the maintenance of cardiac energy balance as well as the state of the heart's extracellular environment (e.g., availability of metabolic fuels). Hypoxic depression of plasma [non-esterified fatty acids] (NEFA), an important cardiac aerobic fuel, is a common response in many species of hypoxia-tolerant fishes, including tilapia. We tested the hypothesis that decreased plasma [NEFA] is important for maintaining stable cardiac function during and following hypoxia exposure, based on the premise that continued reliance upon cardiac fatty acid metabolism under such conditions could impair cardiac function. We examined the effect of severe hypoxia exposure (PO2 < 0.2 kPa) on routine and maximum performance of the in situ perfused tilapia heart under conditions of routine (400 μmol L(-1)) and low (75 μmol L(-1)) [palmitate], which mimicked the in vivo levels of plasma [NEFA] found in normoxic and hypoxic tilapia, respectively. Under both concentrations of palmitate, the in situ tilapia heart showed exceptional hypoxic performance as a result of a high maximum glycolytic potential, confirming our previous results using a perfusate without fatty acids. We additionally provide evidence suggesting that non-contractile ATP demand is depressed in tilapia heart during hypoxia exposure. Cardiac performance during and following severe hypoxia exposure was unaffected by the level of palmitate. Thus, we conclude that hypoxic depression of plasma [NEFA] in fishes does not play a role in cardiac hypoxia tolerance.

We examined the control of breathing and respiratory gas exchange in six species of high-altitude duck that independently colonized the high Andes. We compared ducks from high-altitude populations in Peru (Lake Titicaca at ∼3800 m above sea level; Chancay River at ∼3000-4100 m) with closely related populations or species from low altitude. Hypoxic ventilatory responses were measured shortly after capture at the native altitude. In general, ducks responded to acute hypoxia with robust increases in total ventilation and pulmonary O 2 extraction. O 2 consumption rates were maintained or increased slightly in acute hypoxia, despite ∼1-2°C reductions in body temperature in most species. Two high-altitude taxayellow-billed pintail and torrent duckexhibited higher total ventilation than their low-altitude counterparts, and yellow-billed pintail exhibited greater increases in pulmonary O 2 extraction in severe hypoxia. In contrast, three other high-altitude taxa-Andean ruddy duck, Andean cinnamon teal and speckled tealhad similar or slightly reduced total ventilation and pulmonary O 2 extraction compared with low-altitude relatives. Arterial O 2 saturation (S aO2) was elevated in yellow-billed pintails at moderate levels of hypoxia, but there were no differences in S aO2 in other high-altitude taxa compared with their close relatives. This finding suggests that improvements in S aO2 in hypoxia can require increases in both breathing and haemoglobin-O 2 affinity, because the yellow-billed pintail was the only high-altitude duck with concurrent increases in both traits compared with its low-altitude relative. Overall, our results suggest that distinct physiological strategies for coping with hypoxia can exist across different high-altitude lineages, even among those inhabiting very similar high-altitude habitats.