Abstract
West, John B. High altitude limits of living things. High Alt Med Biol. 22:342–345, 2021.—The tolerance of animals to high altitude is generally limited by the low partial pressure of oxygen (P
Introduction
It is well known that animals, plants, and other living things are limited in their tolerance to high altitude. Bert (1878) was one of the first scientists to emphasize the importance of hypoxia. In this study, we look briefly at a variety of species in the animal and plant kingdoms, to compare the ability of individual species to exist at extreme altitudes.
Animals
Human beings
It is appropriate to start with humans at the highest altitude on earth, that is the summit of Mt. Everest at 8,848 m. A remarkable coincidence is that this highest point in the world appears to be right at the limit of human tolerance to hypoxia. The available evidence suggests that if the summit was only a few 100 m or so higher, it would be impossible for climbers to reach it breathing air. This conclusion is based on the reports of Messner (1979) and Habeler (1979) who were the first climbers to reach the Everest summit without supplementary oxygen. It is clear from their accounts that near the summit, both men were right at the limit of their physical activity. This might remind us of other cosmic coincidences such as the fact that the diameter of the moon is just sufficient to cause a total eclipse of the sun.
It is true that at the present time, large numbers of climbers reach the Everest summit every year, but they can only do this by breathing supplementary oxygen. It was not until 1968, after some 42 years of humans attempting to climb the mountain, that Messner and Habeler reached the summit while breathing air. This remains an exceptional feat although remarkably, Sherpa Ang Rita has accomplished it 10 times.
Other humans have spent substantial periods of time at very high altitudes while breathing air. A notable example was the caretakers of the Aucanquilcha sulfur mine in north Chile. In 1986, there were two men at an altitude of 5,950 m, barometric pressure 373 mmHg, who had been living there continuously for 2 years. They were apparently the highest inhabitants of the world (West, 1986). The mine is now closed.
Another example of prolonged exposure to high altitude was the participants of the 1960–1961 Silver Hut Himalayan expedition led by Edmund Hillary. They lived for several months at an altitude of 5,800 m, barometric pressure 380 mmHg. These were lowlanders who were studying the physiological changes that occur during prolonged exposure to very high altitude. However, the conclusion was that it would be impossible for these men to live for much longer at this altitude, partly because of the relentless loss of weight (Pugh, 1962). These observations accord with the highest permanent settlement in the world being La Rinconada, a mining town more than four decades old in the eastern Peruvian Andes at 5,100 m (West, 2002).
Mammalian Fetuses
The mammalian fetus must be able to tolerate very low levels of oxygen. The British physiologist Joseph Barcroft once famously referred to the environment of the fetus as “Everest in utero,” and subsequent measurements have confirmed this (Barcroft, 1935). For example, the partial pressure of oxygen (PO2) in the descending aorta of a sheep fetus is about 25 mmHg, whereas that based on the alveolar PO2 in a climber on the Everest summit is predicted to be similar (West et al., 1982) and even as low as 19 mmHg in a climber with an arterial blood sample drawn just below summit (Grocott et al., 2009).
Measurements have been made on the fetus of the llama (Lama glama) comparing this with the sheep and showing the llama's advantages in very hypoxic conditions (Llanos et al., 2003). Fetal tolerance and normal growth with this magnitude of hypoxia may rest in part on fetal hemoglobin as is the strategy of many high altitude mammals and other vertebrates that either have hemoglobins with intrinsic high O2 affinity (low P50) or alter concentrations of small molecular allosteric effectors of hemoglobin O2 affinity to accomplish more O2 binding and delivery to tissues.
Other mammals
Recently a group of leaf-eared mice (Phyllotis xanthopygus rupestris) were reported living at an altitude of about 6,700 m on an extinct volcano in the Andes (Storz et al., 2020). It is thought that their food was small insects. These are the highest mammals that have been described to date. Deer mice (Peromyscus maniculatis) are found at many lower altitudes in North America.
Some other mammals can live at very high altitudes. An example is the Tibetan goa (Procapra picticaudata) that lives up to an altitude of about 5,750 m. Other animals that can live at high altitude include the yak (Bos grunniens), which can be found up to an altitude of 6,000 m, and is well known to trekkers in the Everest region because it is used to carry loads to the Everest base camp. Yaks have been shown to have an increased concentration of hypoxia-inducible factor-1 in their brain, lung, and kidney (Qiang Qiu et al., 2012).
Birds
Several species of birds fly at very high altitudes. The best known is the bar-headed goose (Anser indicus) that migrates over the Himalayas (Scott et al., 2015). This animal spends the summers in Mongolia or Tibet, and the winters in low-land India. It has been seen as high as 7,000 m, although there is some speculation on whether it actively flies to this attitude, or whether it takes advantage of updrafts.
There have been several accounts of collisions between birds and aircraft at very high altitudes. The most dramatic was a collision between an aircraft and a Ruppells griffon (Gyps rueppellii) at the extreme altitude of 37,000 ft (11,300 m) over Abijan, Ivory Coast, in western Africa in 1973. After the collision the engine was shut down and the aircraft landed safely. The remains of the bird in the engine allowed the species to be accurately identified (Manville, 1963). Another collision was an aircraft with a Mallard (Anas platyrhyncos) at an altitude of 21,000 ft (6,400 m) near Battle Mountain, Nevada, in 1962. Again, identification of the species was based on the feathers (Manville, 1963). As in the case of the bar-headed geese, there is a question of whether these birds were actively flying at these high altitudes, or whether they were taken up by wind currents.
Fishes
These face special challenges of hypoxia at high altitude because the oxygen content of water even at sea level is a small fraction of that of air. For example, about 21% of air is oxygen, that is there is 210 ml of oxygen in a liter of air. By contrast, a liter of water contains only about 5 ml of oxygen at sea level because of the low solubility of oxygen. As the PO2 in the air decreases with increasing altitude, so the PO2 in the water does the same. A further difficulty is that in many lakes, the PO2 decreases with depth because oxygen is consumed by other fish and some forms of vegetation.
Nevertheless, there are lakes at high altitude that contain fish. One of the largest is the alkaline Lake Qinghai in western China at an altitude of 3,205 m. The most abundant fish is the naked carp (Gymnocyprus przwalski), which in addition to hypoxia must deal with the stress of defending itself against an ambient water pH of 10 (Matey et al., 2008).
Amphibians and reptiles
These vertebrates inhabit many of the same high altitude locales even as high as 5,000 m (Subba, 2010; Esquerre et al., 2019).
Insects
Many insects can be found at high altitudes although because they are so small, there is often a question of whether they choose this or whether they are simply swept up by the atmospheric conditions. Some butterflies are known to fly at high altitudes in their annual migration. For example, Monarchs (Danaus plexippus) are known to spend periods at altitudes of 3,350 m in their long migration between North and South America, and in the Bolivian Andes, a butterfly (Piercolias fosteri) is found at 4,200 m. It is also known that some species of bumble-bees are able to fly at simulated altitudes exceeding those of Mt. Everest (Dillon and Dudley, 2014). During the British Everest expedition of 1924, the naturalist Hingston described a group of jumping spiders (Euophrys omnisuperstes) that he found at an estimated altitude of 22,000 ft (6,700 m). This means that these animals may be at the same altitude as that of the leaf eared mice referred to earlier. In fact, Hingston concluded that spiders are “the highest inhabitants of the earth” (Hingston, 1925).
Primitive invertebrates
Some primitive animals can survive extremely harsh conditions, including very high altitudes. In some instances, it is difficult to know if the organism is alive or dead. For example, is a bacterial spore that is not metabolizing alive or dead? Under some circumstances it can be revived.
One of the most florid examples of a primitive invertebrate is the tardigrade (Ecdysozoa).
These have been collected from the summits of very high mountains where the cold temperatures and hypoxia are extreme. They are eight-legged segmented micro-animals that live in water (Fig. 1). Their length is only from 0.05 to 1.22 mm. Some of these animals were exposed to the hard vacuum of space for 10 days in low earth orbit and survived with no subsequent differences compared with controls. Two species were tested, namely Milnesium tardigradum and Richtersius coronifer. These studies showed that these primitive animals can survive hypoxic conditions that are fatal to all other animals (Jonsson et al., 2008). This animal likely wins the prize for tolerance to extreme prolonged hypoxia.
Tardigrade (Milnesium tardigradum). This organism has an extreme tolerance to hypoxia. It can survive the hard vacuum of space and dehydration where the PO2 is essentially zero for many days (Jönsson et al., 2008). PO2, partial pressure of oxygen.
A recent twist in this story is that a payload of material including a large number of tardigrades that were heading for the moon in an Israeli mission planned crash landed on it on April 5, 2021. Whether any of the organisms reached the moon is not known, but the extreme hardiness of these animals raises the possibility that they could survive. This also raises the interesting question of whether similar animals could survive on exoplanets or Mars, and perhaps the present mission to Mars will throw light on this.
Plants
These comprise the enormous family of other living things on earth as correctly recognized by the author of Genesis in his initial verses 11 and 20. Here we should distinguish between vascular and nonvascular plants. The former is those we see every day in our gardens or fields and include trees. The term vascular refers to the liquid conduits for xylem and phloem that these plants have. Xylem conducts nutrients up the plant from the roots, whereas phloem conducts the products of photosynthesis down. Examples of nonvascular plants include mosses and liverworts. Lichens are usually not considered plants.
There are many obvious differences between animals and plants that are relevant to high altitude (Humboldt and Bonpland, 2009). First, animals can move to a more favorable environment if necessary, whereas plants are fixed. Also, animals depend on oxygen that diminishes as altitude increases, but plants use photosynthesis that depends on light, and the availability of carbon dioxide, which also falls in equal proportion. Light generally increases with altitude. There are other technical factors that are relevant (Gale, 2004). As the barometric pressure falls, the diffusion rate of water vapor rises, and this increases transpiration rates from the leaves. These rates may become very high as altitude increases and the result may be interference with the diffusion of carbon dioxide into the leaf, which compounds the effect of the lower partial pressure of carbon dioxide on rates of photosynthesis (Billings and Godfrey, 1967). Finally, plants utilize oxygen in the dark and underground in a process called dark respiration (Rawat and Purohit, 1991), and thus may be stressed and disadvantaged by high altitude hypoxia (Sakata and Yokai, 2002).
Vascular plants have been found at altitudes >6,000 m in the Himalayas. In 1935 and 1952, two expeditions attempting to climb Mt. Everest collected vascular plants at an estimated altitude of 6,400 m (Dentant, 2018). The identity of one of these specimens (Saussurea gnaphalodes) was determined immediately after the expeditions. This is a thistle-like plant that can grow to a meter in height and is not uncommon in the Himalayas. The name comes from the alpinist Horace Benedict de Saussure who was an early climber on Mount Blanc. Only recently were the four other specimens identified (Dentant, 2018).
In 2012, six vascular plants were discovered in a single patch at an altitude of 6,150 m on the summit of Mount Shukule II in Ladakh (Angel et al., 2016). The plants included Draba alshehbazii, which is apparently limited to Eastern Ladakh. The authors suggested that an important factor in the elevation was the microbial community in the roots that may have been dispersed by wind, and that global warming may have played a role.
Moss, a nonvascular plant, was apparently collected at an estimated altitude of 6,480 m on Mt. Everest in 2011 by Benegas et al. (2011), but few details are available.
Lichens are not plants but are composite organisms that arise from cyanobacteria living among filaments of multiple fungi species. They are very hardy and are found all over the world at all altitudes. Experiments in which samples are exposed to the hard vacuum and radiation of low earth orbit in space confirm their hardiness (Raggio et al., 2011; Sancho et al., 2007).
Footnotes
Acknowledgment
I thank Zhenxing Fu for assistance with the figure.
Author Disclosure Statement
No competing financial interests exist.
Funding Information
Funding was provided by UCSD.