Sara Östlund-Nilsson

Does size matter for hypoxia tolerance in fish

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.

Hypoxia in paradise: widespread hypoxia tolerance in coral reef fishes

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.

Effects of elevated temperature on coral reef fishes: loss of hypoxia tolerance and inability to acclimate

Water temperature is expected to rise on coral reefs due to global warming. Here, we have examined if increased temperature reduces the hypoxia tolerance of coral reef fish (measured as critical [O(2)]), and if temperature acclimation in adults can change the resting rate of O(2) consumption and critical [O(2)]. Two common species from Lizard Island (Great Barrier Reef, Australia) were tested, Doederleins cardinalfish (Ostorhinchus doederleini) and lemon damselfish (Pomacentrus moluccensis). In both species, a 3 degrees C rise in water temperature caused increased oxygen consumption and reduced hypoxia tolerance, changes that were not reduced by acclimation to the higher temperature for 7 to 22 days. Critical [O(2)] increased by 71% in the cardinalfish and by 23% in the damselfish at 32 degrees C compared to 29 degrees C. The higher oxygen needs are likely to reduce the aerobic scope, which could negatively affect the capacity for feeding, growth and reproduction. The reduced hypoxia tolerance may force the fishes out of their nocturnal shelters in the coral matrix, exposing them to predation. The consequences for population and species survival could be severe unless developmental phenotypic plasticity within generations or genetic adaptation between generations could produce individuals that are more tolerant to a warmer future.

From record performance to hypoxia tolerance: respiratory transition in damselfish larvae settling on a coral reef

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.

Coward or braveheart: extreme habitat fidelity through hypoxia tolerance in a coral-dwelling goby

SUMMARY Coral reef fishes are not known for their hypoxia tolerance. The coral-dwelling goby, Gobiodon histrio, rarely leaves the shelter of its host coral colony. However, our measurements indicate that this habitat could become hypoxic on calm nights ([O2] minima=2–30% of air saturation) due to respiration by the coral and associated organisms. Moreover, at very low tides, the whole coral colony can be completely air exposed. Using closed respirometry in water, we found that G. histrio maintains O2 uptake down to 18% of air saturation, and that it can tolerate at least 2 h at even lower O2 levels. Furthermore, during air exposure, which was tolerated for more than 3 h, it upheld a rate of O2 consumption that was 60% of that in water. The hypoxia tolerance and air breathing abilities enables this fish to stay in the safety of its coral home even when exposed to severe hypoxia or air. To our knowledge, this is the first report of hypoxia tolerance in a teleost fish intimately associated with coral reefs.

Tribute to P. L. Lutz: respiratory ecophysiology of coral-reef teleosts.

SUMMARY One of the most diverse vertebrate communities is found on tropical coral reefs. Coral-reef fishes are not only remarkable in color and shape, but also in several aspects of physiological performance. Early in life, at the end of the pelagic larval stage, coral-reef fishes are the fastest swimmers of all fishes in relation to body size, and show the highest specific rates of maximum oxygen uptake. Upon settling on the reef, coral-reef fishes have to adopt a demersal lifestyle, which involves coping with a habitat that can become severely hypoxic, and some fishes may even have to rely on air breathing when their coral homes become air exposed. Oxygen availability appears to be a major ambient selection pressure, making respiratory function a key factor for survival on coral reefs. Consequently, hypoxia tolerance is widespread among coral-reef fishes. Hypoxia can even be a factor to gamble with for those fishes that are mouthbrooders, or a factor that the coral inhabitants may actively seek to reduce by sleep-swimming at night. Here, we summarize the present knowledge of the respiratory ecophysiology of coral-reef teleosts. From an ecophysiological perspective, the coral reef is an exciting and largely unexplored system for testing existing hypotheses and making new discoveries.

Hypoxia tolerance and air-breathing ability correlate with habitat preference in coral-dwelling fishes

Hypoxia tolerance and air-breathing occur in a range of freshwater, estuarine and intertidal fishes. Here it is shown for the first time that coral reef fishes from the genera Gobiodon, Paragobiodon and Caracanthus, which all have an obligate association with living coral, also exhibit hypoxia tolerance and a well-developed air-breathing capacity. All nine species maintained adequate respiration in water at oxygen concentrations down to 15–25% air saturation. This hypoxia tolerance is probably needed when the oxygen levels in the coral habitat drops sharply at night. Air-breathing abilities of the species correlated with habitat association, being greatest (equaling oxygen uptake in water) in species that occupy corals extending into shallow water, where they may become air exposed during extreme low tides. Air-breathing was less well-developed or absent in species inhabiting corals from deeper waters. Loss of scales and a network of subcutaneous capillaries appear to be key adaptations allowing cutaneous respiration in air. While hypoxia tolerance may be an ancestral trait in these fishes, air-breathing is likely to be a more recent adaptation exemplifying convergent evolution in the unrelated genera Gobiodon and Caracanthus in response to coral-dwelling lifestyles.

Shrimps remove ectoparasites from fishes in temperate waters

We have found that two very common species of North Atlantic shallow water shrimp, Palaemon adspersus and Palaemon elegans, remove and feed on ectoparasites on plaice (Pleuronectes platessa L.). The relationship could be mutualistic, as we did not observe any attempts by the fishes to feed on the shrimps. The ectoparasites removed included monogenean worms (Gyrodactylus sp.) and sea lice (Lepeophtheirus pectoralis). An experiment showed that there were 65% more Gyrodactylus parasites on the fishes that had been apart from compared with those that had been together with shrimps for 48 h. Shrimps on coral reefs are known for cleaning fishes, but that shrimps in temperate waters show parasite-cleaning behaviour is, to our knowledge, a new observation.

Hypoxia Tolerance in Coral Reef Fishes

Publisher Summary This chapter discusses some examples of hypoxic coral reef habitats and hypoxia-tolerant coral reef inhabitants, and suggests that hypoxia tolerance is a widespread phenomenon among coral reef fishes. Because coral reefs have the highest biodiversity of any marine habitat, finding hypoxia tolerance there could mean that there is an exceptional wealth of hypoxia adaptations waiting to be explored in this ecosystem. The best-studied hypoxia tolerant vertebrates, which include North American freshwater turtles, carps, and goldfish, have all evolved their hypoxia tolerance to allow overwintering in hypoxic habitats at temperatures close to 0 °C. By contrast, coral reef fishes live at a water temperature near 30 °C. This is not far from the body temperature of homeothermic vertebrates like mammals. Thus, to disclose the mechanisms that coral reef fishes have evolved to allow hypoxic survival could be of particular relevance for biomedical hypoxia and ischemia research. The only relatively well-studied example of a hypoxia-tolerant reef fish is the epaulette shark on Heron Island, which becomes preconditioned to hypoxia during subsequent nights of nocturnal low tides. Recent studies indicate that hypoxia tolerance is widespread among coral reef teleosts, including damselfishes, cardinalfishes, gobiids, and blennids. A case study on a coral-dwelling goby indicates that hypoxia tolerance, as well as air breathing, are prerequisites for this species to stay in the shelter of their coral homes indefinitely.