Maximum running speed of captive bar-headed geese is unaffected by severe hypoxia

Abstract

While bar-headed geese are renowned for migration at high altitude over the Himalayas, previous work on captive birds suggested that these geese are unable to maintain rates of oxygen consumption while running in severely hypoxic conditions. To investigate this paradox, we re-examined the running performance and heart rates of bar-headed geese and barnacle geese (a low altitude species) during exercise in hypoxia. Bar-headed geese (n = 7) were able to run at maximum speeds (determined in normoxia) for 15 minutes in severe hypoxia (7% O2; simulating the hypoxia at 8500 m) with mean heart rates of 466±8 beats min-1. Barnacle geese (n = 10), on the other hand, were unable to complete similar trials in severe hypoxia and their mean heart rate (316 beats.min-1) was significantly lower than bar-headed geese. In bar-headed geese, partial pressures of oxygen and carbon dioxide in both arterial and mixed venous blood were significantly lower during hypoxia than normoxia, both at rest and while running. However, measurements of blood lactate in bar-headed geese suggested that anaerobic metabolism was not a major energy source during running in hypoxia. We combined these data with values taken from the literature to estimate (i) oxygen supply, using the Fick equation and (ii) oxygen demand using aerodynamic theory for bar-headed geese flying aerobically, and under their own power, at altitude. This analysis predicts that the maximum altitude at which geese can transport enough oxygen to fly without environmental assistance ranges from 6,800 m to 8,900 m altitude, depending on the parameters used in the model but that such flights should be rare.

Figure 1. Experiment set up for bar-headed goose respirometry.

Heart rate (f _H) was recorded both externally using an ADI BioAmp with subcutaneous electrodes and internally using custom made loggers (see methods). Temperature (T°) and relative humidity (RH) were measured inside the respirometer and used to correct flow rate through the respirometer to STPD conditions (see methods). Subsamples of well-mixed air from the respirometer (fan indicated as cross in circle) were first dried (- H₂O) before analysis of fractional concentration of CO₂ and O₂ in a gas analyser. Analyser data was passed via a PowerLab to a computer. To create conditions of hypoxia, appropriate amounts of N₂ were flowed into the respirometer. Arterial (a) and mixed venous (v) blood samples were taken through cannulae exiting the lid of the respirometer.

Figure 2. Heart rate and metabolic rate of bar-headed geese.

(a) Mean heart rate, (b) Mean (in mL.min⁻¹) and Mean (in mL.min⁻¹) of un-cannulated bar-headed geese against increasing treadmill speed in normoxia (solid line) and hypoxia (dashed line in part a), error bars show s.e.m.; Lines show linear models for fit, error bars show ±1 s.e.m.

Figure 3. The effect of exercise and hypoxia on blood gases.

Bar plots showing the effect of exercise and hypoxia on arterial and mixed venous (a) oxygen content, (b) (c) and for bar-headed geese. Values at rest (Re) and during running (Ex) are shown for normoxia (white bars) and severe hypoxia (7% O₂; grey bars). Bars show mean values, error bars show 1 s.e.m., a =  mean values are significantly different at rest, b =  mean values are significantly different to normoxia, where p<0.05.

Figure 4. The effect of exercise and hypoxia on lactate, haematocrit and haemoglobin.

Box plots showing mixed venous (a) blood lactate, (b) haematocrit and (c) haemoglobin for bar-headed geese at rest (white boxes) and during running (grey boxes) in normoxia and hypoxia (fractional concentration of O₂ indicated on x-axis). * shows values that are significantly different to values at rest, + shows values that are significantly different to normoxia, where p<0.05.

Figure 5. Modelling maximum flight altitude.

(a) the relationship between body mass and heart mass for 21 bar-headed geese (circles) and 22 barnacle geese (triangles) from captive collections (white symbols) and the wild (several weeks prior to migration; black symbols), solid line shows linear model (R² = 0.65), dashed lines show confidence interval, unpublished data. (b) Oxygen-haemoglobin dissociation curve showing data collected from bar-headed geese in normoxia (black symbols) and hypoxia (white symbols); present study data are shown as circles, data from Fedde et al. as triangles and P₅₀ from Meir & Milsom and Petschow et al. (blood in vitro at 41°C and 4% CO₂, approximating pH 7.4) shown as a white square. Curves are fitted to in-vivo data collected in the present study in normoxia (line labelled ‘a’); data collected in the present study in severe hypoxia (line labelled ‘b’) and to data published by Fedde et al. (line labelled ‘c’), excluding four outliers at high . A curve is also fitted to in-vitro data published by Petschow et al. and Meir & Milsom (dashed line, labelled ‘d’). (c) Plot showing the modelled increases in demand (black line) during horizontal flight at high altitude and the reduction in potential O₂ supply (one black line, two dashed grey lines) by the cardiovascular system. The supply models use the oxygen-haemoglobin dissociation curves in part b (curve a, labelled ‘supply a’; grey dashed curve b, labelled ‘supply b’ and grey dashed curve d labelled ‘supply c’). Grey vertical line approximates the summit of Mount Everest at 8,848 metres. Predicted supply crosses demand at 7,850 m (supply ‘a’), 8,300 m (supply ‘b’) and 8,900 m (supply ‘c’).