Marine elasmobranchs such as shark, dogfish and rays overcome their osmotic difficulties in a unique way. They have a similar chloride content to marine teleosts and at first sight one would expect them to be much the same position, with body fluids hypotonic to the surrounding sea water. However, the body fluids of marine elasmobranch are slightly hypertonic to sea water. Surprisingly, this is achieved by retaining the nitrogenous waste product urea so that the osmotic pressure of the body fluids is raised to the point that it slightly exceeds that of the surrounding sea water. The result of this on the marine elasmobranch is a slight influx of water which is readily expelled by the kidney. The importance of retaining urea is that it eliminates the need of having to swallow sea water and eliminate excess salts.
The retention of urea in marine elasmobranchs is made possible by its reabsorption in the kidney tubules, together with the fact that the gills are impermeable to it. The remarkable thing is that the tissues can withstand it. Normally, a high concentration of urea alters the shape of proteins by breaking the hydrogen bonds linking adjacent polypeptide chains. This can completely disrupt the smooth functioning of cells, particularly when enzymes are affected. Marine Elasmobranch proteins are immune to these effects. Indeed the tissues appear to thrive on urea. Interestingly, if the heart of a marine elasmobranch is perfused with a balanced salt solution lacking the usual high concentration of urea, it will stop beating!
Osmoregulatory Mechanisms in Marine Elasmobranchs
The survival of marine elasmobranch is at risk. Many species, particularly those with short seasonal life cycles, suffer from water quality degradation that may be beyond their ability to cope.
Despite their low body fluid salt concentrations elasmobranchs are able to maintain a slightly hypertonic state with seawater. This is achieved by the addition of organic solutes, primarily urea, to their body fluids.
Since the pioneering contributions of Homer Smith in 1930s, much has been learned about osmoregulatory mechanisms in marine elasmobranchs. Most species of elasmobranchs maintain their body fluid osmolality slightly above that of sea water, with this being primarily due to the retention of urea.
Plasma urea concentrations are about a quarter to one-third of the concentration of salt in sea water. Urea retention enables a continuous osmotic influx of water across semi-permeable membranes (e.g., gills).
A substantial portion of this osmotic inflow is made up of ions including sodium (Na) and chloride (Cl) but not magnesium or sulfate. The osmotic balance is further regulated by the secretion of intestinal HCO3-, which liberates free hydrogen ions (H+) into the blood. In addition, some osmotic regulation is accomplished through the excretion of non-protein amino acids such as taurine and betaine from liver, skeletal muscle and red blood cells (RBC). A variety of studies suggest that the initial composition of a fish’s gastrointestinal microbiome is affected by development mode or environmental exposure.
Marine elasmobranchs retain large amounts of urea in the blood and body fluids, raising the osmolality of their body water above that of seawater. This high osmolality also facilitates free water uptake across the gills. Urea at these relatively high concentrations destabilizes proteins and must be counteracted by stabilizing solutes, such as trimethylamine oxide (TMAO) and betaine. The ratio of urea to these solutes is typically 2:1, and this osmotic strategy is used from an early stage in embryo development.
Urea losses across the gills in elasmobranchs are much lower than in teleost fish, presumably because of a specialized urea transport protein and a cholesterol content inserted into gill cell membrane phospholipids. Injection of NH4Cl causes acidosis in teleost fishes, but this does not occur in elasmobranchs, suggesting that the pH of their blood is maintained by a metabolic and/or transport mechanism rather than by passive diffusion across the gills. The low diversity of the intestinal microbiome in elasmobranchs may be due to a sparsity of biochemical niches, or to a strong environmental filtering effect.
The osmotic regulation of elasmobranchs involves the secretion of urea and excretion of salts from the rectal gland. These actions help maintain a hyper-osmotic relationship with their environment and prevent ionic imbalance. This is accomplished through a series of steps in the gills, kidneys and liver. These steps are important to maintain the acid-base balance and ionic consistency of a shark’s body fluids.
The renal glomerulus is an important step in urine formation, which occurs when permeable capillaries leak water, salts, glucose and small proteins into Bowman’s capsule. The tubules then selectively add or remove solutes and water to turn the general blood filtrate into urine waste.
Elasmobranchs may also have a blood microbiome that can provide novel antibiotic compounds to combat bacterial, fungal and parasitic infections. Identifying these microorganisms and understanding the interactions between them and elasmobranch physiology will allow for a deeper understanding of the health of sharks, skates and rays and lead to better practices in managed care.
Marine elasmobranchs (sharks, skates and rays) are important components of marine ecosystems. However, their populations are declining worldwide and their conservation is challenging. This collection provides access to a broad range of articles that address all aspects of elasmobranch biology and ecology, from basic to applied research.
Most elasmobranchs are stenohaline, but some species can enter freshwater and become marginally euryhaline (for example, the Atlantic stingray Potamotrygon motoro). The osmoregulatory mechanisms used by these species must be modulated to accommodate differences in salinity.
In order to better understand the osmoregulatory strategies of these species, we analyzed the kidney urea transporters of elasmobranchs. Using comparative biochemistry and molecular techniques, we found that the transporters of the spiny dogfish Squalus acanthias and the rat UT-A2 are homologous.
We demonstrated that the urea loss across the gills of elasmobranchs is much lower than in teleost fish, due to the presence of an active urea transporter in the gills and a unique composition of gill cell membranes with exceptionally high cholesterol inserted into the phospholipid bilayer. This modification reduces the passive diffusion of small solutes such as urea, which is lost to seawater down a concentration gradient.