Fish cover a large size range, from milligrams to tonnes, and many of them are regularly exposed to large variations in ambient oxygen levels. For more than half a century, there have been various, often divergent, claims regarding the effect of body size on hypoxia tolerance in fish. Here, we attempt to link old and new empirical data with the current understanding of the physiological mechanisms behind hypoxia tolerance. Three main conclusions are drawn: (1) body size per se has little or no impact on the ability to take up oxygen during hypoxic conditions, primarily because the respiratory surface area matches metabolic rate over a wide size range. If size-related differences are seen in the ability for oxygen uptake in a species, these are likely to reflect adaptation to different life-styles or habitat choice. (2) During severe hypoxia and anoxia, where fish have to rely on anaerobic ATP production (glycolysis) for survival, large individuals have a clear advantage over smaller ones, because small fish will run out of glycogen or reach lethal levels of anaerobic end-products (lactate and H(+)) much faster due to their higher mass-specific metabolic rate. (3) Those fish species that have evolved extreme adaptations to hypoxia, including haemoglobins with exceptionally high oxygen affinities and an alternative anaerobic end-product (ethanol), reveal that natural selection can be a much more powerful determinant of hypoxia tolerance than scaling of physiological functions.

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Using respirometry, we examined the hypoxia tolerance of 31 teleost fish species (seven families) inhabiting coral reefs at a 2-5 m depth in the lagoon at Lizard Island (Great Barrier Reef, Australia). All fishes studied maintained their rate of oxygen consumption down to relatively severe hypoxia (20-30% air saturation). Indeed, most fishes appeared unaffected by hypoxia until the oxygen level fell below 10% of air saturation. This, hitherto unrecognized, hypoxia tolerance among coral reef fishes could reflect adaptations to nocturnal hypoxia in tide pools. It may also be needed to enable fishes to reside deep within branching coral at night to avoid predation. Widespread hypoxia tolerance in a habitat with such an extreme biodiversity as coral reefs indicate that there is a wealth of hypoxia related adaptations to be discovered in reef fishes.

The fastest swimming fishes in relation to size are found among coral reef fish larvae on their way to settle on reefs. By testing two damselfishes, Chromis atripectoralis and Pomacentrus amboinensis, we show that the high swimming speeds of the pre-settlement larvae are accompanied by the highest rates of oxygen uptake ever recorded in ectothermic vertebrates. As expected, these high rates of oxygen uptake occur at the cost of poor hypoxia tolerance. However, hypoxia tolerance is needed when coral reef fishes seek nocturnal shelter from predators within coral colonies, which can become severely hypoxic microhabitats at night. When the larvae settle on the reef, we found that they go through a striking respiratory transformation, i.e. the capacity for rapid oxygen uptake falls, while the ability for high-affinity oxygen uptake at low oxygen levels is increased. This transition to hypoxia tolerance is needed when they settle on the reef; this was strengthened by our finding that small resident larvae of Acanthochromis polyacanthus, a damselfish lacking a planktonic larval stage, do not display such a transition, being well adapted to hypoxia and showing relatively low maximum rates of oxygen uptake that change little with age.