David M. Larson
Every year in Mass Audubon's Birder's Certificate Program, when I am presenting information about avian physiology, I mention the amazing phenomenon of the migration of Bar-headed Geese. These birds migrate between their wintering and nesting grounds over the Himalayan Mountains and Tibetan Plateau, at 5000–6000 meters (approximately 16,000–20,000 feet), and have been seen in flight at almost 7300 meters (24,000 feet). In comparison, human mountain climbers commonly use bottled oxygen above 7000 meters. Combining the metabolic demands of flapping flight (already metabolically expensive), the greater exertion required to fly in the lower air pressure at altitude (thinner air requires faster flight to maintain lift), and the decreased oxygen concentration at altitude, makes flying to this level pretty impressive.
So how do these geese manage? One key is the efficiency of the avian respiratory and cardiovascular systems. Birds can extract more oxygen from the air they breathe and get rid of more carbon dioxide than mammals can, due to the anatomy of their respiratory system. Avian hearts empty more fully upon contraction and are thus more efficient. Against this backdrop, Meir, et al. (2019) tested respiratory and cardiac parameters in Bar-headed Geese that had been trained to fly in a wind tunnel while hooked up to a hose and mask that supplied air of normoxic (21% oxygen = sea level), moderately hypoxic (10.5% oxygen = 5,500 meters), and severely hypoxic (7% oxygen = 9,000 meters) conditions. The breathing masks contained sensors to measure oxygen and carbon dioxide levels in inspired and expired air. In-dwelling catheters measured arterial and mixed venous dissolved oxygen at rest, pre-flight, and steady-state flight under the three oxygen concentrations.
Birds flying in normoxic conditions extracted more oxygen and released more carbon dioxide than birds at rest. This means that under increased demand, the respiratory system worked at a higher level in flying birds. Heart rate (<150 beats per minute at rest and >300 beats per minute in flight) and wing beat rate (five times per second) did not differ significantly in flight under the three atmospheric oxygen concentrations.
The amount of dissolved oxygen in venous blood in steady-state flight dropped rapidly at the start of flight. It decreased in all atmospheric conditions, but was lower in hypoxia than in normoxia. This result suggests increased oxygen extraction by working muscle. Under preflight conditions, arterial blood oxygen levels decreased with hypoxia. During flight, similar arterial oxygen levels were maintained at each of the three air supply concentrations. This result suggests that the geese have excess respiratory gas exchange capacity.
In conjunction with the available literature, the authors conclude that their study geese increased their metabolic rate 16-fold in flight over resting levels. This increase is supported by an increase in oxygen transported per heartbeat and a modest 2.5-fold increase in heart rate. Clearly, this species has significant cardiac reserves, because heart rates during hypoxic flight were not increased over normoxic flight. The authors conclude that hypoxic flight is supported by a general decrease in metabolic rate during flight compared to normoxic flight. The mechanisms for decreased metabolic rate in hypoxic flight remain untested. Possibilities include oxygen limitation (unlikely), suppression of metabolism in nonflight-related tissues (likely), increased mechanical efficiency of flight (likely), or a switch to anaerobic metabolism (unlikely during the duration of these flights).
An interesting finding of this study was the decrease in venous temperature during flight. This blood temperature change could be due to evaporative cooling in the respiratory system. Cooled blood would have a higher oxygen loading capacity in the lungs. As the blood warms in the active flight muscles, it would release that oxygen where it is needed for the working tissue. This is an interesting hypothesis worthy of further study.
This project provides a fascinating window on the physiology of Bar-headed Geese when flying at high altitudes under hypoxic conditions. There are, of course, several caveats of note. These geese were imprinted on humans and trained to fly under decidedly odd conditions (rubber mask, hose, catheters, wind tunnel). Given the conditions and despite their training, their flights with instrumentation lasted only a few minutes before they, presumably, decided to stop. In contrast, it takes wild geese eight hours to fly over the Himalayan Mountains, so the physiological demands and response would certainly change during a flight of that duration. And those wild geese face low air pressures (hypobaria) at altitude, in addition to hypoxia. Hypobaric conditions make the birds work harder to maintain altitude and forward motion due to reduced lift at low air pressures. Indeed, the stress of hypobaria could be more physiologically significant than that of hypoxia. So the experiments in this study shed incremental light on the question of how geese fly at high altitudes. In addition, only one of their geese was willing to fly consistently in severe hypoxic conditions, and then only briefly. As the authors point out, this bird could have had unusual characteristics, so the severe hypoxia data are hanging from a thin thread.
The development of backpack instrumentation capable of measuring oxygen and carbon dioxide levels in arterial and mixed venous blood, blood temperature, and heart rate, combined with transmitting the data to a satellite system, could go a long way toward explaining the physiological demands and the response of the geese to migratory flight under hypoxic and hypobaric conditions.
Reference
- Meir, J.U., J.M. York, B.A. Chua, W. Jardine, L.A. Hawkes, and W.K. Milsom. 2019. Reduced metabolism supports hypoxic flight in the high-flying bar-headed goose (Anser indicus). eLife 8:e44986. DOI: https://doi.org/10.7554/eLife.44986.
David M. Larson, PhD, is the Science and Education Coordinator at Mass Audubon's Joppa Flats Education Center in Newburyport, the Director of Mass Audubon's Birder's Certificate Program and the Certificate Program in Bird Ecology (a course for naturalist guides in Belize), a domestic and international tour leader, President of the Nuttall Ornithological Club, and a member of the editorial staff of Bird Observer.