FERG
Fish Endocrinology Research Group
Endocrine Control of Elasmobranch osmoregulation
Elasmobranch fish (sharks, skates and rays) are found in a variety of habitats, ranging from full seawater to full freshwater. The osmotic challenges imposed on the animals in these different environments are distinct. Furthermore, the life cycle of some elasmobranchs, such as the bullshark, Carcarhinus leucas, involve migration between freshwater and seawater. All elasmobranchs possess similar endocrine and osmoregulatory organs.

Additional osmotic challenges placed on some elasmobranchs are concerned with feeding habits. For example, the European Lesser Spotted dogfish, Scyliorhinus canicula, feeds primarily on invertebrates, and tends to gorge feed. This imposes a high salt load on the animal introducing an acute osmotic challenge.

European Lesser Spotted Dogfish
European Lesser Spotted Dogfish (Scyliorhinus canicula). Image from Tricas et al. (1997) Sharks and Rays, Harper Collins, London.
We have investigating the endocrine and physiological mechanisms in the adaptation of a number of elasmobranch species to varying environmental salinities, and the maintenance of salt and water balance in the face of changing dietary inputs.

Elasmobranchs adapted to seawater employ a hyperosmotic strategy, in which the plasma osmolality is maintained slightly higher than that of the surrounding medium. Elevation of blood plasma osmolality is maintained by the retention of urea and methylamine compounds such as trimethylamine oxide (TMAO). However, an concentration gradient, from seawater to blood plasma, for sodium and chloride ions still exists.

Osmolyte regulation in a typical elasmobranch

Therefore, ionic regulation is required through the integrated response of a variety of tissues and glands. The principle tissues involved in this response in elasmobranchs are, the gill, kidney, gut and rectal gland.

Gill: Elasmobranch gills are extremely impermeable to urea and indeed, the permeability coefficient for urea in the elasmobranch gill epithelia is reported to be one of the lowest in the animal kingdom. The mechanism behind this impermeability is unclear and it has been suggested that this effect is due to a ‘physical barrier’ to urea. Despite this apparent physical barrier the gills are still the greatest site for net loss of urea. As with the kidney the gills are another important site for the regulation of sodium and chloride in the elasmobranch. However, unlike teleosts the elasmobranch gill does not have the capacity to produce a greater efflux than influx of sodium and chloride ions. Therefore, during periods of osmotic challenge the gill epithelia alone cannot efficiently maintain a constant balance of salts and water in the animal.

Kidney: The length and complexity of the functional unit of the elasmobranch kidney, the nephron, has almost certainly hindered scientific understanding of renal function. However, the retention of urea at the nephron is undoubtedly one reason for its huge complexity. Whether this process is entirely active or passive has yet to be determined. Using an in situ perfused renal preparation we have demonstrated renal effects of a number of peptide hormones, including arginine vasotocin (AVT), angiotensin II (Ang II) and C-type natriuretic peptide (CNP). AVT and Ang II have similar effects, causing a reduction in urine flow rate and glomerular filtration rate (GFR). This reduction in GFR was due to a decrease in the filtering population of nephrons. CNP caused an increase in urine flow rate and GFR, but no increase in the filtering population of nephrons. However, elasmobranch fish do not have the capacity to produce a concentrated urine. Therefore, in the face of a sudden osmotic challenge the elasmobranch cannot maintain osmoregulatory balance through kidney function alone.

Gut: The role of the gut in elasmobranch osmoregulation was thought to be relatively insignificant. However, recent research by FERG has demonstrated that this may not be the case, especially during adaptation to different environmental salinities. Classically elasmobranchs were thought not to drink due to the hyperosmotic strategy that they employ. Work carried out by FERG in collaboration with Prof. Yoshio Takei in Tokyo demonstrated that transfer of the Japanese dogfish, Triakis scyllia, from 75% to 100% salinity induced a drinking response. Recent work has demonstrated a similar effect in S. canicula.

Rectal gland: Pictured right is a cross section through a corrosion cast of the rectal gland of the, S. canicula. The gland is situated at the posterior end of the abdominal cavity, is fed by a single vessel, the rectal gland artery, and empties via a central duct into the intestine close to the rectum. The rectal gland is a highly specialised salt secreting organ that secretes a fluid that is isosmotic to blood plasma but is almost entirely composed of sodium and chloride. This aspect of the gland makes it an ideal model tissue for the study of epithelial sodium and chloride transport. FERG has concentrated on investigating hormonal influences on rectal gland secretion; rectal gland activity following feeding; and rectal gland activity in varying environmental salinities.

Research carried out by FERG, in collaboration with Prof. Mike Conlon, has demonstrated that a peptide derived from the gut of S. canicula, Scyliorhinin II, stimulates secretion from the rectal gland. It is possible that there is an integrative response between the gut and rectal gland in response to a salt/volume load following feeding. The exact mechanisms of this response have yet to be determined.

The renin-angiotensin system (RAS) is pictured left. In mammals, renin, produced in the juxtaglomerular apparatus in the kidney, acts on a protein substrate angiotensinogen, produced in the liver, to form the decapeptide angiotensin I (Ang I). Angiotensin converting enzyme (ACE) then cleaves Ang I to form the octapeptide and biologically active component angiotensin II (Ang II). The principle role of Ang II is the control of blood volume. In mammals it has been shown to be, dipsogenic (induces thirst), vasopressor (constricts blood vessels), anti-diuretic (reduces the production of urine) and anti-natriuretic (sodium reabsorptive). Until recently the evolution of the RAS was considered to have occurred first in teleost fishes and the more ancient elasmobranchs were thought not to possess a RAS. Using the European lesser spotted dogfish, Scyliorhinus canicula, and the Japanese dogfish, Triakis scyllia, as model elasmobranchs FERG has determined that elasmobranchs do in fact possess a RAS, and furthermore, Ang II appears to exert similar influences as found in mammals.