Hypoxia in fish
Fish respond to hypoxia with varied behavioral, physiological, and cellular responses to maintain homeostasis and organism function in an oxygen-depleted environment.
[1] Therefore, hypoxia survival requires a coordinated response to secure more oxygen from the depleted environment and counteract the metabolic consequences of decreased ATP production at the mitochondria.
The membrane hypothesis was proposed for the carotid body in mice,[13] and it predicts that oxygen sensing is an ion balance initiated process.
The mitochondrial hypothesis was also proposed for the carotid body of mice, but it relies on the levels of oxidative phosphorylation and/or reactive oxygen species (ROS) production as a cue for hypoxia.
[26] Behavioural adaptations meant to survive when oxygen is scarce include reduced activity levels, aquatic surface respiration, and air breathing.
[27] Other examples of fishes that reduce their activity levels under hypoxia include the common sole,[28] the guppy,[29] the small-spotted catshark,[30] and the viviparous eelpout.
[40] One study looked at 26 species representing eight families of non-air breathing fishes from the North American great plains, and found that all but four of them performed ASR during hypoxia.
[41] Another study looked at 24 species of tropical fish common to the pet trade, from tetras to barbs to cichlids, and found that all of them performed ASR.
[43][44][45] Some species may show morphological adaptations, such as a flat head and an upturned mouth, that allow them to perform ASR without breaking the water surface (which would make them more visible to aerial predators).
In the tambaqui, a South American species, exposure to hypoxia induces within hours the development of additional blood vessels inside the lower lip, enhancing its ability to take up oxygen during ASR.
ABOs are modified gastrointestinal tracts, gas bladders, and labyrinth organs;[54] they are highly vascularized and provide additional method of extracting oxygen from the air.
Temperature also affects the speed at which the gills can be remodelled: for example, at 20 °C in hypoxia, the crucian carp can completely remove its ILCM in 6 hours, whereas at 8 °C, the same process takes 3–7 days.
[60] The ILCM is likely removed by apoptosis, but it is possible that when the fish is faced with the double stress of hypoxia at high temperature, the lamellae may be lost by physical degradation.
[60] The naked carp, a closely related species native to the high-altitude Lake Qinghai, is also able to remodel their gills in response to hypoxic conditions.
In response to oxygen levels 95% lower than normoxic conditions, apoptosis of ILCM increases lamellar surface area by up to 60% after just 24 hours.
[63] Fish exhibit a wide range of tactics to counteract aquatic hypoxia, but when escape from the hypoxic stress is not possible, maintaining oxygen extraction and delivery becomes an essential component to survival.
Maintaining oxygen extraction and delivery to the tissues allows continued activity under hypoxic stress and is in part determined by modifications in two different blood parameters: hematocrit and the binding properties of hemoglobin.
[68] During chronic hypoxia exposure, the mechanism used to increase hematocrit is independent of the spleen and results from hormonal stimulation of the kidney by erythropoetin (EPO).
[65] The oxygen binding affinity of hemoglobin (Hb-O2) is regulated through a suite of allosteric modulators; the principal modulators used for controlling Hb-O2 affinity under hypoxic insult are: In rainbow trout as well as a variety of other teleosts, increased RBC pH stems from the activation of B-andrenergic Na+/H+ exchange protein (BNHE) on the RBC membrane via circulating catelcholamines.
The net influx of Na+ ions and the compensatory activation of Na+/K+-ATPase to maintain ionic equilibrium within the RBC results in a steady decline in cellular ATP, also serving to increase Hb-O2 affinity.
[73] As a further result of inward Na+ movement, the osmolarity of the RBC increases causing osmotic influx of water and cell swelling.
[65] Intertidal hypoxia-tolerant triplefin fish (Family Tripterygiidae) species seem to take advantage of intracellular acidosis and appears to "bypasse" the traditional oxidative phosphorylation and directly drives mitochondrial ATP synthesis using the cytosolic pool of protons that likely accumulates in hypoxia (via lactic acidosis and ATP hydrolysis).
[75] Several species of African cichlids raised from early stage development under either hypoxic or normoxic conditions were contrasted in an attempt to compare Hb isoforms.
The ability to decrease energy demand by metabolic suppression is essential to ensure hypoxic survival due to the limited efficiency of anaerobic ATP production.
Metabolic suppression also reduces the accumulation rate of deleterious anaerobic end-products (lactate and protons), which delays their negative impact on the fish.
[86][87] The few studies that have used calorimetry reveal that some fish species employ metabolic suppression in hypoxia/anoxia (e.g., goldfish, tilapia, European eel) while others do not (e.g. rainbow trout, zebrafish).
If the hypoxic exposure lasts sufficiently long, the fish will succumb to a depletion of its glycogen stores and/or the over-accumulation of deleterious anaerobic end-products.
Furthermore, the severely limited energetic scope that comes with a metabolically suppressed state means that the fish is unable to complete critical tasks such a predator avoidance and reproduction.
[90] In addition to a reduction in the rate of protein synthesis, it appears that some species of hypoxia-tolerant fish conserve energy by employing Hochachka's ion channel arrest hypothesis.
[98] The second prediction has been more difficult to prove experimentally, however, indirect measures have showed a decrease in Na+/K+-ATPase activity in eel and trout hepatocytes during hypoxic conditions.
