One of the most characteristic observations during the algal bloom mortality is the appearance of varying degrees of blushing – red blotchy skin – in many of the rays and sharks (elasmobranchs) that have washed up.
This is a very peculiar phenomenon, for which there is no clear cut explanation. Much of the research my colleagues and I did over 30 years was on the control of the blood circulation in the skin, mostly in mammals. In mammals like humans, this type of skin flushing is due to the small blood vessels in the skin (the capillaries) becoming leaky, so that blood cells, both red and white, end up in spaces between the cells of affected tissues. This is called extravasation and it is a normal part of an inflammatory response to injury or infection: it is the painful redness in the skin after sunburn or an insect sting or whatever.
LEFT: Normal skin showing the tooth-like denticles (dark grey outlines) embedded in the dermis with dermal blood vessels (red lines). The thin epidermis (pale grey line) forms the outer impermeable layer of the skin. RIGHT: Flushing of he skin around the base of the denticles must be due to blood leaking from the small blood vessels (broken red lines) around the bases of the denticles in the dermis and perhaps also from blood vessels in the denticles themselves.
Like all vertebrates, the outer surface of the skin consists of a specialised layer epithelial cells, the epidermis. Beneath the epidermis is the dermis, a thicker layer containing small blood vessels, nerves, and other tissues all embedded in a tough connective tissue that provides strength the skin. The dermis also gives rise to the scales that protrude through the epidermis to provide the characteristic outer surface of the skin1.
The scales of elasmobranchs are very different in structure from the scales of other fish and are called placoid scales or denticles. “Denticle” means “little tooth” which is a great name, since their underlying structure is almost the same as teeth2. They have a hard outer layer made of dentine and enamel-like vitrodentine with a soft inner pulp containing small blood vessels and other tissue components. As well as providing physical protection, the denticles are arranged in such a way that they streamline the flow of water over the skin during swimming, thereby reducing water resistance and making swimming much more efficient that it would otherwise be3.
If we examine closely with a macro photography set-up the flushed skin of a freshly washed up shark or ray, we can see that the blood has accumulated around the bases of the denticles in the skin. The most likely source of the blood around the bases of the denticle is via leakage (ie extravasation) from the capillaries in the skin and perhaps the denticle themselves. But how can this happen?
The main toxic action of Karenia mikimotoi, one of the dominant species in the algal bloom, is to cause cytolysis as a result of disrupting the surface membrane of cells it contacts. If those cells are red blood cells, they will burst and spill out their red haemoglobin: this is haemolysis, a different phenomenon to extravasation. It is difficult to see how a cytolytic agent could enter the blood stream via the gills and then act on only some regions of the circulation. You would expect such an action to be most dominant in the regions of the circulation closest to the gills and this is clearly not the case in the elasmobranchs.
In looking for an explanation, several important observations need to be kept in mind:
•• only some of the sharks and rays that have washed up show flushing.
•• the amount of flushing varies considerably: some individuals have only a small amount in one or two areas of skin; others have extensive areas around the head, belly, fins and tail.
•• flushing has been seen in individuals that have been washed up while still alive, so it is not a post-mortem phenomenon such as blood pooling.
•• based on its known properties and molecular targets, brevetoxin, produced by the other dominant species in the bloom, Karenia cristata, cannot be responsible for these effects.
There are three possible explanations for these observations, none of which is fully satisfactory. The real situation may be some combination of all of them or it may be something else altogether…
1. Skin damage. The cytolytic action of Karenia directly damages the epidermal cells in the skin between the denticles and thereby accesses the microcirculation of the skin, leading to extravasation first, and then possibly haemolysis, around the bases of the denticles.
Perhaps Karenia directly affects the skin.
The surface epithelium of the skin (epidermis) is disrupted (grey broken line) by the cytolytic action of Karenia which can then reach the blood vessels. The cytolytic action of Karenia then breaks down the walls of the blood vessels in the skin (red broken lines) so they become permeable and blood leaks out into the surrounding tissues.
The problem with this explanation is that shark skin is remarkably resistant to damage4. The epidermis maintains a thin layer of protective mucus5 that would tend to restrict direct contact between Karenia and the surface of the skin, thereby reducing the likelihood of cytolysis. Injuries to shark skin, from bites of other animals, for example, are resistant to infection and heal quickly6. Despite the obvious flushing of the skin, there are no signs of direct skin damage such as sloughing or ulceration.
2. Vascular inflammation. Another possibility is that some component of Karenia enters the blood stream via the damaged epithelium and capillaries of the gills and then sets off an inflammatory response in the skin, similar to a skin rash that people can develop in an allergic reaction. This response requires a complex set of interactions between the immune system and vascular system, involving many types of cells and biochemical signalling systems. Elasmobranchs have most, but not all, of this system of responses7.
Maybe Karenia enters the blood stream via the gills and generates an inflammatory vascular reaction.
The surface epithelium of the skin remains intact (epidermis, grey line). Following an inflammatory reaction (yellow stars) to Karenia, or some part of it, the walls of the blood vessels in the skin become permeable to blood cells (red broken lines) allowing them to leak out into the surrounding tissues.
3. Systemic infection. The flushing could be the result of a reaction to a systemic blood infection. Sea water always harbours a wide variety of potentially infectious microorganisms, most notably bacteria and viruses. But bacteria proliferate greatly in a harmful algal bloom, feeding off the remains of the dinoflagellates themselves as well as the organisms killed by the bloom. In addition, proliferation of some bacteria may be enhanced by the same climatic and oceanographic conditions that are causing the bloom itself8.
Sharks and rays have a well developed immune system and systemic infection seems to be rare9. The mucus on their skin harbours complex communities of bacteria and viruses that mostly provide protection from pathological infection10. However, even minor cytolytic damage to the gills could allow pathogenic microorganisms in the water to enter the blood stream. Once in the blood, the microorganisms could proliferate to a degree that overwhelms the immune system leading to sepsis (blood poisoning) and consequential vasculitis (inflammation of the blood vessels). Indeed, such as reaction has been observed in fish with gill damage due to a bloom dominated by diatoms11 and in sharks infected with Vibrio bacteria12. There are potentially two main ways such a condition could generate flushing in the skin:
•• The immune system responds to the infection in an aberrant way, leading to massive inflammation in parts of the circulation. As in the case of a reaction to Karenia, described above, the walls of the small blood vessels in the skin become permeable to the blood cells, which then leak out into the surrounding tissues.
•• The infectious microorganisms themselves have cytolytic and haemolytic actions, leading to blood cells breaking and leaking into surrounding tissues. Many bacteria have these properties, including some known to exist in marine environments, such as some Vibrio species. These effects are likely to be independent of any direct actions of the dinoflagellates.13
Could a reaction to systemic bacterial infection cause the flushing?
Having entered the blood via Karenia-damaged gills, pathogenic bacteria (dark rods) either generate an extreme inflammatory reaction in small blood vessels of the skin, or the bacteria themselves are cytolytic and haemolytic. In either case, the blood vessel wall break down (broken red lines) and blood can leak into the tissues surrounding the denticles.
An explanation like this is consistent with the observation that only some sharks and rays show flushing: they would be individuals that have experienced both the necessary level of Karenia-induced gill damage to allow infection, but not immediate death, and exposure to sufficient numbers of infectious microorganisms that can generate this reaction. The patchy nature of the flushing in any individual may be the result of randomness in levels of infection established in various parts of the circulation.
Testing any of these potential explanations requires analytical microscopic examination of affected tissues, to determine exactly where cytolytic damage has occurred, whether or not the pooled blood shows haemolysis, and whether or not there are signs of bacterial infection.
Skin flushing seems to be largely restricted to some sharks and rays. Nevertheless, something similar is occasionally observed in other types of fish. The range of potential explanations is the same.
Selected references
- Akat B et al (2021) Comparison of vertebrate skin structure at class level: A review. Anatomical Record 305: 3543-3608, https://doi.org/10.1002/ar.24908
↩︎ - Cooper RL et al (2022) Teeth outside the mouth: The evolution and development of shark denticles. Evolution & Development 23: 54-72, https://doi.org/10.1111/ede.12427 ;
Nicklin EF et al (2024) Evolution, development, and regeneration of tooth-like epithelial appendages in sharks. Developmental Biology 516: 221-236, https://doi.org/10.1016/j.ydbio.2024.08.009
Klimley AP (2013) The Biology of Sharks and Rays. University of Chicago Press, https://press.uchicago.edu/ucp/books/book/chicago/B/bo11018459.html
↩︎ - Ankhelyi MV et al (2018) Diversity of dermal denticle structure in sharks: Skin surface roughness and three-dimensional morphology. Journal of Morphology 279: 1132-1154, https://doi.org/10.1002/jmor.20836 ;
Gabler-Smith MK et al (2021) Dermal denticle diversity in sharks: novel patterns on the interbranchial skin. Integrrative Organsimal Biology 3: obab034, https://doi.org/10.1093/iob/obab034
↩︎ - Hagood ME et al (2023) Relationships in shark skin: mechanical and morphological properties vary between sexes and among species. Integrative and Comparative Biology 63: 1154-1167, https://doi.org/10.1093/icb/icad111
↩︎ - Bachar-Wikstrom E et al (2023) Identification of novel glycans in the mucus layer of shark and skate skin. International Journal of Molecular Sciences 24: 14331, https://doi.org/10.3390/ijms241814331 ;
Bachar-Wikstrom E et al (2023) Mass spectrometry analysis of shark skin proteins. International Journal of Molecular Sciences 24: 16954, https://doi.org/10.3390/ijms242316954 ;
Doane MP et al (2023) The epidermal microbiome within an aggregation of leopard sharks (Triakis semifasciata) has taxonomic flexibility with gene functional stability across three time‑points. Microbial Ecology 85: 747-764, https://doi.org/10.1007/s00248-022-01969-y
Fischer MJ et al (2025) Slippery and smooth shark skin: how mucus transforms surface texture. Journal of Morphology 286: e70046, https://doi.org/10.1002/jmor.70046
Perry CT et al (2021) Elasmobranch microbiomes: emerging patterns and implications for host health and ecology. Animal Microbiome 3: 61, https://doi.org/10.1186/s42523-021-00121-4 ;
Ritchie KB et al (2017) Survey of antibiotic-producing bacteria associated with the epidermal mucus layers of rays and skates. Frontiers in Microbiology 8: 1050, https://doi.org/10.3389/fmicb.2017.01050
↩︎ - Chin A et al (2015) Blacktip reef sharks (Carcharhinus melanopterus) show high capacity for wound healing and recovery following injury. Conservation Physiology 3: cov062, https://doi.org/10.1093/conphys/cov062
Heath B et al (2025) Are sutures a pathway to infection? A multidisciplinary assessment of wound healing in sharks following internal acoustic tagging. Wildlife Research 52: WR25009, https://doi.org/10.1071/WR25009
↩︎ - Bosi G et al (2025) The Leydig organ of elasmobranchs: Shed light on an active and mysterious defense center with immunological characterization of its cells. Tissue and Cell 93: 102755, https://doi.org/10.1016/j.tice.2025.102755 ;
Gargano C et al (2025) Shark immune system: A review about their immunoglobulin repertoire. Fish and Shellfish Immunology 160: 110187, https://doi.org/10.1016/j.fsi.2025.110187
Marra NJ et al (2017) Comparative transcriptomics of elasmobranchs and teleosts highlight important processes in adaptive immunity and regional endothermy. BMC Genomics 18: 87, https://doi.org/10.1186/s12864-016-3411-x
↩︎ - Jeong HJ et al (2010) Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Science Journal 45: 65-91, https://doi.org/10.1007/s12601-010-0007-2 ;
Gong W et al (2017) Molecular insights into a dinoflagellate bloom. The ISME Journal 11: 439-452, https://doi.org/10.1038/ismej.2016.129
↩︎ - Garner MM (2013) A retrospective study of disease in elasmobranchs. Veterinary Pathology 50: 377-389, https://doi.org/10.1177/0300985813482147
Smith NC et al (2019) A comparison of the innate and adaptive immune systems in cartilaginous fish, ray-finned fish, and lobe-finned fish. Frontiers in Immunology 10: 2292, https://doi.org/10.3389/fimmu.2019.02292
Also see references in [7] above.
↩︎ - Kerr EN et al (2023) Stingray epidermal microbiomes are species-specific with local adaptations. Frontiers in Microbiology 14: 1031711, https://doi.org/10.3389/fmicb.2023.1031711
Ritchie KB et al (2017) Survey of antibiotic-producing bacteria associated with the epidermal mucus layers of rays and skates. Frontiers in Microbiology 8: 1050, https://doi.org/10.3389/fmicb.2017.01050
↩︎ - Briones V et al (2010) Haemorrhagic septicaemia by Aeromonas salmonicida subsp. salmonicida in a Black-tip Reef Shark (Carcharhinus melanopterus). Journal of Veternary Medicine, Series B 45: 443-445, https://doi.org/10.1111/j.1439-0450.1998.tb00814.x ;
Catanase G & Grau A (2023) First detection of Photobacterium spp. in acute hemorrhagic septicemia from the nursehound shark Scyliorhinus stellaris. Fishes 8: 128, https://doi.org/10.3390/fishes8030128
Grimes DJ et al (1984) Vibrio species as agents of elasmobranch disease. Helgoländer Meeresuntersuchungen 37: 309-317.
Roberts SD et al (2019) Marine heatwave, harmful algae blooms and an extensive fish kill event during 2013 in South Australia. Frontiers in Marine Science 6: 610, https://doi.org/10.3389/fmars.2019.00610 ;
Zhang XH & Austin B (2005) Haemolysins in Vibrio species. Journal of Applied Microbiology 98: 1011-1019, https://doi.org/10.1111/j.1365-2672.2005.02583.x
↩︎ - Clauss TM et al (2008) Hematologic disorders of fish. Veterinary Clinics – Exotic Animal Practice 11: 445-462, https://www.researchgate.net/publication/230801423_Hematologic_disorders_of_fish
Zhang XH et al (2020) Vibrio harveyi: a serious pathogen of fish and invertebrates in mariculture. Marine Life Sciences & Technology 2: 231-245, https://doi.org/10.1007/s42995-020-00037-z
↩︎ - De Rijcke M et al (2016) Toxic dinoflagellates and Vibrio spp. act independently in bivalve larvae. Fish and Shellfish Immunology 57: 236-242, http://dx.doi.org/10.1016/j.fsi.2016.08.027
Ina-Salwany MY et al (2019) Vibriosis in fish: A review on disease development and prevention. Journal of Aquatic Animal Health 31: 3-22, https://doi.org/10.1002/aah.10045
Zhang XH & Austin B (2005) Haemolysins in Vibrio species. Journal of Applied Microbiology 98: 1011-1019, https://doi.org/10.1111/j.1365-2672.2005.02583.x ↩︎
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