The gills of fish have two critical functions1:
(1) Respiration: taking up oxygen (O2) from the water, transferring it to the blood, and transferring carbon dioxide (CO2) back from the blood to the water.
(2) Salt balance: ensuring that the body fluids and cells of the fish are not overwhelmed by salt (sodium chloride, NaCl) in the sea water.
The structure of gills is complicated and varies in detail between different types of fish. But they all follow the same basic plan.
The heart pumps blood via veins from the rest of the body into the gills. This blood is deoxygenated and contains high levels of carbon dioxide (CO2) due to the metabolic activities of all the body tissues, such as muscles, gastrointestinal tract, reproductive organs, etc. This blood is pumped into four pairs of gill arches. Each gill arch bears rows ofgill filaments and each filament is covered by rows of thin ridges called gill lamellae. The gill lamellae are covered with a thin layer of epithelial cells and a filled with a network of blood capillaries. The fish pumps oxygenated water over the gills and between the lamellae by a combination of its swimming action and pumping muscles in its mouth and throat. Water enters via the mouth and exits via the gill slit just in front of the pectoral (fore) fins.
The epithelial cells lining the gills and their lamellae are essential to maintaining the structural and functional integrity of the gills. While they must allow the transfer of dissolved oxygen and carbon dioxide between the sea water and the blood, they also must maintain the large differences in salt concentration between the sea water and the body tissues, including the blood.
The gill epithelium mostly consists of a single layer of more or less cuboid shaped epithelial cells. Each epithelial cell acts as a barrier to salt and water transfer. There are also tight impermeable junctions between adjacent cells that further prevent unwanted salt and fluid transfer. Nevertheless, these barriers are imperfect and cannot completely stop salt from entering the tissues of the gills. The epithelial cells of the gills therefore have another critical function: they can actively pump excess salt back out into the sea water, thereby maintaining the correct salt/water balance of the body tissues and blood. Any extra salt that remains is cleared from the blood by the kidneys.
Sharks and rays use a different mechanism to maintain salt balance
Sharks and rays have gills with a structure very similar to that of other fish2. Most do not have pumping muscles in their throat so they need to keep swimming to maintain water movement across their gills. Rather than excreting excess salt out of their blood via their gills, most is removed by the kidneys.
Sharks and rays have higher levels of salt in their body fluids and tissues compared with other fish, about half that of sea water. But they still have a problem of keeping excess salt out of their body. They do this by loading their blood with high concentrations of urea and other soluble compounds.3 Urea is a waste product of protein metabolism. It is closely related chemically to ammonia and rich in nitrogen. Such high levels of urea are toxic to most animals, so it is normally excreted by the kidneys into urine as it is formed. But sharks and rays have a range of mechanisms to protect them from the potentially harmful metabolic effects of urea.
Together with the higher salt levels in the body fluids, the high concentration of urea acts as a kind of buffer against the salt in the sea water. Just as in other fish, for this protection to work, it is vital to maintain the integrity of the epithelial cells of the gills.
Algal cytotoxins disrupt the integrity of gills in fish, sharks and rays
When a fish swims through water containing dinoflagellates such as Karenia mikimotoi or Karenia cristata, they cannot avoid taking them in as the fish passes water in from its mouth and out from its gills. Most fish have a series of mechanisms to keep the gills clear of particles or tiny organisms in the water that could interfere with gill function. But high levels of Karenia overcome these defences as they become trapped and aggregate on and between the structures of the gills4. Once here, their cytotoxic action breaks down the cell membranes of the protective epithelial cells of the gills and the metabolic safety barrier between the body fluids of the fish and the sea water is lost. Reactive oxygen species associated with the membrane breakdown exacerbate the cytolytic effects. It doesn’t take long for the correct salt balance of the fish to be lost, wth fatal consequences. This is just as true for sharks and rays which also need an intact epithelial barrier in their gills to maintain correct levels of salt and urea in the body fluids.
The loss of gill integrity also severely compromises the ability of the gills to transfer oxygen and carbon dioxide between the water and the blood. This becomes even more of a problem in the presence of high densities of microorganisms in the water, since their metabolic activity can greatly reduce the amount of oxygen in the water. Furthermore, bacterial activity associated with the decay of dead organisms can reduce oxygen availability even more.
In fish where gill damage is not enough to cause death, an impaired epithelial barrier potentially could allow more brevetoxin to enter the bloodstream of the fish, adding another possible contribution to fish mortality5. Sublethal exposure to algal cytotoxins also can lead to a long-lasting inflammatory response in gills with can further compromise respiratory function6.
Damaged gills produce excess mucus
One key defence that gills have against particles or micro-organisms that could interfere with gill function is the production of mucus by special populations of epithelial cells. The mucus traps the particles on the surface of the gills and is then swept away by a variety of mechanisms, thereby cleaning the gills. When the mucus-producing cells are actually damaged by irritants such as a cytotoxin, all the mucus that had been stored inside them is dumped out onto the surface of the gills, overwhelming the mechanism that normally sweep the mucus away7. This has two disastrous consequences:
(1) the mucus is so thick it inhibits oxygen and carbon dioxide exchange in areas of the gills that are still functional.
(2) the mucous traps even more Karenia contributing even more cytolytic action and leading to further damage to the gills.
Mucus-like secretions from the Karenia organisms themselves also may contribute to further clogging the gills8.
The following images show two juvenile Bluefin Leatherjackets (Thamnaconus degeni) freshly washed up on beaches south of Adelaide. On the left, there is a marked accumulation of blood-stained mucus around the opening from the gills. The blood in the mucus is a strong indication that the structural integrity of the gills has been severely compromised. On the right, the skin around the gill opening shows localised bleeding, almost certainly the result of cytolytic Karenia organisms that would have been trapped in mucus in the area that has now been washed away.
Why are so many dead juvenile leatherjackets washed up?
Throughout this harmful algal bloom, vast numbers of juvenile leatherjackets have washed up on beaches. Why might this be so? All fish in the Tetraodontiformes group (leatherjackets, toadfish, pufferfish and their allies) have remarkably small external gill openings, with the operculum almost covered with skin9. When combined with their generally slow swimming habits10, there must be relatively slow or restricted water flow over the gills compared with a fish like a whiting. This combination of structure and behaviour in leatherjackets would make them much more susceptible to developing severe gill malfunction due to longer contact times with Karenia further exacerbating the situation.
Although bleeding and skin damage around the gill opening has been most commonly seen in leatherjackets, some other types of fish are occasionally seen with similar lesions.
This video illustrates an example of the number of leatherjackets washed up after a storm during the bloom at Seacliff beach in July 2025..
This video shows the swimming style of this group of fish, in this case a toadfish, photographed at Seacliff in summer 2025, before the bloom.
Damage to leatherjacket eyes
Many of the leatherjackets washed up on the beaches have missing eyes. In November and December 2025, sea conditions were such that juvenile leatherjackets were washed up that were only recently dead. Some of these showed extremely swollen eyes, sometimes accompanied by bleeding in and around the eye socket. In general, bulging eyes, known as exophthalmia, can be caused by many things. It can be common in aquarium fish where it is often called “popeye” which in turn can have several causes, most usually following infection.
The appearance of swollen eyes in freshly washed-up leatherjackets suggests severe inflammation and swelling of the sclera, the outer part of the eyeball which forms the whites of the eyes in humans11. Such fluid accumulation is mostly likely due to inflammation following exposure to cytotoxins in the water, in a similar way to the gills. Any such inflammation could be amplified by the involvement of sensory nerves in the cornea and surrounding tissues12. The damage is possibly further compounded by responses to secondary bacterial infection, similar to the situation in sharks and rays. It is not due to brevetoxin. Indeed, exophthalmia following various types of infection has been reported in a variety of fish types, including those in areas exposed to algal blooms.13
The eyes of fish have a complex relation with the vascular system in order to obtain enough oxygen to function properly. This vascular arrangement shares some key features in common with the gas gland of the swim bladder14 and it is possible this mechanism is also disrupted by exposure to toxins in the bloom, leading to exophthalmia15 (see below for more on possible swim bladder dysfunction).
The swollen eyes would be fragile and very susceptible to damage by impact or abrasion. This is presumably why so many of these fish wash-up with missing eyes. A similar explanation probably also applies to cowfish. Why other types of fish do not seem to be affected this way, or at least nowhere near as severely, is another mystery.
Why are some leatherjackets floating on the surface of the sea?
In addition to large numbers of juvenile leatherjackets washing up dead on beaches, there have been several reports of varying numbers of dead or dying juvenile leatherjackets floating off some of the beaches. There is something odd about these observations…
It’s more or less common knowledge that dead fish often float. This is where the phrase “turning belly up” comes from. The usual explanation for this is that bacteria in the gut of the dead fish start decomposing it, producing gas in the body cavity that then reduces the overall density of the fish so that it now floats.
But at least some of the floating leatherjackets are still alive, so the gas-due-to-decomposition explanation cannot apply here.
Fish are more dense than water, so, in the absence of anything else, they would sink if they stop swimming. But most fish contain a swim bladder that helps to keep them neutrally buoyant so they don’t sink. Via an incredibly complicated mix of physics, chemistry, biochemistry and anatomy, the fish are able to generate gas (mostly oxygen, derived from oxygen in the blood) from specialised gas glands to fill the bladder to varying degrees16. The volume of gas in the bladder can be varied to keep the fish more or less neutrally buoyant as it moves through the water column. Because the gas is compressible, the amount of gas in the bladder needs to be dynamically controlled to keep the fish where it wants to be. Some of this control happens more or less automatically, but it can be modulated by the nervous system.
Some of the freshly washed up leatherjackets have distended bellies that are full of gas. This could be due to dysregulated activity of the gas glands in the swim bladder. Such swelling would only be seen in fresh specimens since the gas would quickly diffuse way once the animals have been dead for a while.
How could the bloom cause this? The gills are critical in maintaining not just the correct levels of oxygen and carbon dioxide in the blood, but also its acid-base balance, as well as its salt levels. If these become abnormal as a result of gill damage from algal cytotoxins, the complex set-up of gas generation in the swim bladder may well be comprised. If the fish have been exposed to brevetoxin, there also could be dysfunction of the neural pathways affecting the control of swim bladder function. Swollen bellies and abnormal swimming behaviour also have been reported in fish as a consequence of bacterial infection17, something that could occur secondary to cytolytic damage to the gills or skin of fish.
Another possibility is that the fish are badly disoriented. All fish have a lateral line organ which detects vibrations in the water (it is closely related to the sensors of the inner ear) and it is used by fish for orientation, especially in relation to other fish in their school. The nerves in the lateral line are very close to the surface of the skin and are probably susceptible to being directly affected by any neurotoxins in the water. Other algal toxins have been shown to affect lateral line function, leading to abnormal orientation and swimming behaviour in affected fish18. So, in principle, brevetoxin could access these nerves in a similar manner leading to abnormal orientation and swimming behaviour. If the fish is unable to maintain its position in the water column due to the effects of the toxins, sudden changes in depth (and therefore ambient pressure) may lead to uncontrolled production of gas in the swim bladder and increased buoyancy.
Selected references
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↩︎ - Pepe-Vargas P et al (2024) Effects of the harmful algal bloom toxin, okadaic acid, on the mechanoreceptors of larval anchoveta (Engraulis ringens) under varying environmental conditions. Frontiers in Marine Science 11: 1446509, https://doi.org/10.3389/fmars.2024.1446509 ↩︎
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