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| 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. |
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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.
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| 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.
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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.
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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. |
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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. |
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