Osmotic and volaemic effects on drinking rate in elasmobranch fish
1
School of Biology, Gatty Marine Laboratory, University of St Andrews, St
Andrews, Fife KY16 8LB, Scotland
2
Ocean Research Institute, University of Tokyo, Tokyo 1648639,
Japan
* e-mail: wga{at}st-andrews.ac.uk
Accepted 28 January 2002
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Summary |
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Key words: elasmobranch, hypovolaemia, hyperosmoraemia, drinking rate, dogfish, Scyliorhinus canicula, Triakis scyllia
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Introduction |
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In the hypo-osmotic environment of fresh water, osmotic gradients favour
the passive entry of water across semi-permeable membranes such as those of
the gills in teleost fish, negating a requirement to drink
(Maetz, 1970). However, in the
hyperosmotic environment of sea water, water is constantly lost and teleost
fish drink to maintain ionic and water balance
(Oide and Utida, 1968
), with
excess ions being excreted at the gills and/or kidney
(Evans, 1993
).
In contrast to marine teleosts, marine elasmobranchs maintain blood plasma
osmolality iso-osmotic or slightly hyperosmotic to sea water
(Smith, 1931). This elevation
in plasma osmolality is achieved through the regulation of three principal
components, Na+, Cl- and urea, with each component
constituting approximately one-quarter to one-third of total plasma osmolality
(900-1000 mosmol kg-1) (Smith,
1936
). The toxicity of urea is counteracted by the retention of
methylamines, in particular trimethylamine oxide (TMAO)
(Yancey and Somero, 1980
). As
a consequence of their iso/hyperosmoregulatory strategy, marine elasmobranchs
experience little osmotic water flux, no risk of dehydration, as experienced
by the hyporegulating marine teleosts and, therefore, no apparent reason to
drink (Schmidt-Nielsen,
1997
).
Although the majority of elasmobranchs are considered stenohaline marine
species, numerous reports have demonstrated that these species successfully
acclimate to varying degrees of salinity within the laboratory
(Burger, 1965;
Hazon and Henderson, 1984
;
Goldstein and Forster, 1971
).
Furthermore, a number of species, such as the bull shark Carcharhinus
leucas and the Atlantic stingray Dasyatis sabina, inhabit both
marine and freshwater environments
(Thorson et al., 1973
;
Piermarini and Evans, 1998
).
The presence of elasmobranchs in a range of aquatic habitats and the ability
of presumed stenohaline marine elasmobranchs to acclimate to dilute sea water
indicates that the group as a whole has, to varying degrees, the physiological
capacity to survive in changing environmental salinities.
The present study investigated a potential role for drinking in marine elasmobranchs during environmental manipulation and the osmotic/volaemic control behind the drinking response. In the first series of experiments, two species of marine elasmobranch, the European lesser-spotted dogfish Scyliorhinus canicula and the Japanese dogfish Triakis scyllia, were subjected to a change in environmental salinity. Drinking rate was monitored in both species acclimated to a reduced environmental salinity of 80 % sea water (SW) and during acute exposure to the hyperosmotic environment of 100 % SW. To determine the physiological trigger for dipsogenesis, a second series of experiments was conducted in which drinking rate was assessed in S. canicula acclimated to 100 % SW during administration of a variety of osmotic and volaemic challenges.
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Materials and methods |
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Surgical procedures
All procedures outlined below were carried out by licensed personnel under
the guidelines set out by the Animals (Scientific Procedures) Act 1986, UK.
Drinking rate was assessed using a preparation similar to that previously
described for teleost fish (Takei et al.,
1998). Dogfish were anaesthetised using tricaine methanesulphonate
(MS-222, 250 p.p.m.) neutralised with sodium bicarbonate (250 p.p.m.). A
ventro-lateral incision into the abdominal cavity was made just posterior to
the pectoral fin. Retraction of the intestine exposed the stomach, oesophagus
and mesenteric artery. The stomach was cannulated using polyethylene tubing
(1.5 mm outer diameter; Portex tubing, Hythe, Kent), and a tight ligature was
placed around the anterior end of the stomach to prevent fluid from entering
via the oesophagus. The oesophagus was then cannulated with tubing of
similar bore, and the mesenteric and coeliac arteries were cannulated using
0.5 mm outer diameter polyethylene tubing to allow for the administration of
reagents and collection of blood samples. The incision was closed with 5-6
gauge silk sutures, and the fish were allowed to recover in individual
flow-through aquaria (401) at ambient temperature (16-18 °C) for a minimum
of 24 h. During times of rest, the oesophageal and stomach cannulae were
linked to allow imbibation of water and thus the maintenance of body fluid
homeostasis. For the experiments involving S. canicula, the
oesophageal and stomach cannulae were disconnected, fluid imbibed was
collected through the oesophageal cannula into pre-weighed vials, and the
volume of fluid was assessed gravimetrically assuming a specific gravity of 1.
The volume drunk was then replaced into the animal via the stomach
cannula. For the experiments involving T. scyllia, the volume of
fluid imbibed through the oesophageal cannula was assessed by a drop counter,
and the volume of fluid drunk was returned to the fish automatically by a
pulse injector synchronised with the drop counter.
Series 1: salinity challenge
In the salinity challenge experiments, T. scyllia and S.
canicula were stepwise acclimated to 80 % salinity in their respective
aquaria (755 mosmol kg-1 at the Gatty Marine Laboratory, 772 mosmol
kg-1 at Misaki Marine Station) in a manner similar to that
described previously (Tierney et al.,
1998). Briefly, fish were held in acclimation tanks for a minimum
of 3 days, after which the salinity of the water was adjusted to 90 % for the
following 3 days, with the final reduction to 80 % occurring 3 days later.
Once at 80 % SW, the fish were left to acclimate for a minimum of 2 weeks
prior to surgery. Following a minimum of 2 h of assessment of basal drinking
rate at 80 % SW, 100 % SW was introduced into the experimental tanks, with a
complete water change occurring within 30 min. Drinking rate was then assessed
in both species as they acclimated to the increase in environmental
salinity.
Blood samples (0.5 ml) were taken from the coeliac arterial cannulae using pre-chilled syringes 0 and 1.5 and 6 h after the introduction to 100 % SW. Each blood sample was centrifuged at 1300 g for 1 min, and the plasma was removed and assessed for plasma osmolality (Roebling Osmometer, Camlab, Cambridge, UK) and for Cl- (Corning 925 Cl- analyser), Na+ (Corning 480 flame photometer) and urea (Sigma kit no. 640) levels. An equivalent volume of isotonic Ringer was injected into the fish via the mesenteric arterial cannula immediately after a blood sample had been taken.
Series 2: osmotic and volaemic challenge
Only S. canicula was used in series 2. Fish of mixed sex, mean
mass 0.64±0.33 kg (mean ± S.E.M., N=15), acclimated to
100 % SW and held in a manner similar to that described above were used for
the osmotic and volaemic challenge experiments. Surgical procedures were as
described above, and all reagents were purchased from Sigma Chemical Company
(Poole, Dorset, UK). The osmotic stimuli [2 mol l-1 mannitol, 2.19
mol l-1 sucrose (75 %, w/v) and 3.4 mol l-1 NaCl (20 %,
w/v)] were administered at a dose of 1 ml kg-1 body mass to produce
a theoretical percentage cellular dehydration of 0.36, 0.33 and 0.47 %
respectively. Each treatment was made up in dogfish Ringer (in mmol
l-1): NaCl, 240; KCl, 7.0; CaCl2, 10.0;
MgCl2, 4.9; NaHCO3, 2.3;
Na2HPO4.2H2O, 0.5;
Na2SO4, 0.5; urea, 360; trimethylamine oxide, 60 (pH
7.6). In addition, controlled haemorrhaging of 2.5 ml of blood from the
coeliac arterial cannula was carried out, constituting 5.7±0.29 % (mean
± S.E.M., N=6) of total blood volume in the experimental fish
(Thorson, 1962). Blood samples
from the experimental fish were taken in a manner similar to that described
above at 0, 0.5 and 3 h after treatment and analysed for the variables
described above.
Statistical analyses
In series 1 experiments, both species demonstrated a delay in the drinking
response following the introduction of 100% SW. Furthermore, the individual
variation in this delay was considerable. Therefore, mean (±1 S.E.M.)
maximal drinking rates for both species (ml h-1 kg-1)
were assessed as the maximum volume of fluid imbibed over a single 30 min
period during acclimation to 100% SW and compared with basal drinking rate in
80% SW.
For series 2 experiments, values are presented as mean (±1 S.E.M.) drinking rates (ml h-1 kg-1), which were assessed over 20 min periods following manipulation of the experimental fish. Comparisons were made with basal drinking rates prior to injection of test substances or haemorrhaging of the fish. All osmolalities and body fluid osmolyte concentrations were compared with basal values in each respective experimental group. Statistical assessment of the data was carried out using analysis of variance (ANOVA) followed by Tukey's post-hoc test with a Student's t-test to provide a final level of significance.
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Results |
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For both species, plasma osmolality was not significantly higher than basal values until 6h after 100% SW had been introduced into the holding tanks (Table 1). A significant increase in plasma Na+ concentration was observed at 1.5 and 6h after the introduction of 100% SW (Fig. 2). However, plasma Cl- concentration did not match plasma Na+ concentration until 6h after the introduction of 100% SW. This delay in increase in plasma Cl- concentration in the present study is difficult to explain. Plasma urea levels in S. canicula 6h after the introduction of 100% SW did not show a significant change from the concentration observed in fish acclimated to 80% SW (Fig. 2), demonstrating a delay in the increase in plasma urea levels during acclimation in comparison with plasma Na+ and Cl- levels.
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Series 2: osmotic and volaemic challenge
Drinking rates in S. canicula treated with 2 mol l-1
mannitol (1 ml kg-1 body mass), 75% sucrose (1 ml kg-1
body mass) and vehicle (1 ml kg-1 body mass) were not significantly
different from basal values assessed just prior to the administration of the
test substances (Fig. 3B-D).
However, following injection of 20% NaCl (1 ml kg-1 body mass),
drinking rates were found to be significantly lower than basal values 60 min
post-injection (Fig. 3A). With
the exception of plasma Na+ concentration, which was significantly
lower 30 min after injection of 75% sucrose
(Fig. 4C), plasma osmolality
and plasma osmolyte concentrations did not differ from basal values following
administration of the test substances
(Table 2;
Fig. 4).
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Controlled haemorrhaging of 2.5 ml from the experimental fish produced a rapid and profound dipsogenic response: drinking rate was 36 times greater than basal levels within 20 min of haemorrhaging (Fig. 5). This significant response was sustained for a total of 40 min and returned to basal levels within 2 h of haemorrhaging. Plasma concentrations of Na+, Cl- and urea and plasma osmolality did not differ from basal concentrations after haemorrhaging of the fish (Table 2; Fig. 6).
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Discussion |
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Differences in drinking rate with respect to environmental salinity have
previously been reported in S. canicula using a radio-labelled tracer
technique. Basal values were significantly lower and higher in media more
dilute and more concentrated, respectively, than the control of 100% SW
(Hazon et al., 1999). The
drinking responses observed in the present study were maximal between 2-3 and
3-6 h after the introduction of 100% SW in S. canicula and T.
scyllia, respectively, and in general occurred prior to the observed
increase in plasma osmolality at 6 h. The delay in maximal drinking response
contrasts with the rapid and predictable responses observed during transfer
from a dilute to a concentrated environment for a variety of teleosts such as
the Japanese eel Anguilla japonica
(Hirano, 1974
;
Takei et al., 1988
), the
flounder Platichthys flesus
(Carrick and Balment, 1983
) and
the rainbow trout Onchorhynchus mykiss
(Shehadeh and Gordon,
1969
).
The differences in maximal responses observed in the present study, with
that of T. scyllia being nearly 3.5 times greater than that of S.
canicula, may be reflected in the ambient temperatures of the two
aquaria. During experimentation, water temperature was 24-26°C at Misaki
Marine Biological Station and 16-18°C at the Gatty Marine Laboratory.
Interestingly, a temperature-related variation in drinking rate has previously
been reported for the flounder and Japanese eel
(Carroll et al., 1994;
Takei and Tsukada, 2001
). The
differences between the two species used in the present study may also reflect
a difference in their osmoregulatory capacity. Indeed, the elasmobranchs
Heterodontus portusjacksoni and Trygonoptera testacea both
inhabit similar estuarine environments in New South Wales, Australia. However,
T. testacea was recently reported to have greater control of salt and
water balance in dilute environments, indicating a greater osmoregulatory
capacity than H. portusjacksoni
(Cooper and Morris, 1998
).
Despite the differences between the two species observed from salinity
challenge experiments in the present study, it is clear that both have a
physiological requirement to drink the external medium under the appropriate
environmental conditions.
Drinking studies in mammals have demonstrated that intravascular
administration of hypertonic osmotically active solutions, causing
hyperosmoraemia and thus drawing water from the cellular compartment, induces
a profound dipsogenesis (Fitzsimons,
1979,
1998
). Similar experiments in
teleost fish have produced conflicting results. Intra-arterial administration
of hypertonic solutions of NaCl and sucrose were shown to inhibit drinking in
freshwater-acclimated Anguilla japonica
(Takei et al., 1988
). However,
the same study demonstrated a concomitant increase in plasma angiotensin II
concentration, which seemed paradoxical given the potent dipsogenic action of
angiotensin II in these fish (Takei et
al., 1979
). The cause of the inhibition was elucidated by Kaiya
and Takei (1996
): following
injection of hypertonic mannitol and NaCl solutions, there was a transient
increase in plasma levels of atrial (ANP) and ventricular (VNP) natriuretic
peptide. ANP is known to act as an anti-dipsogen in eels and mammals
(Brenner et al., 1990
;
Tsuchida and Takei, 1998
);
indeed, the dose of ANP required to induce anti-dipsogenesis in eels was
reported to be 100 times less than the dipsogenic dose required for
angiotensin II (Takei, 2000
).
These reports could in part explain the inhibition of drinking, at least in
eels, following intra-arterial administration of hypertonic solutions. This
agrees with a non-specific effect of hyperosmoraemia leading to hypervolaemia
acting as a stimulus for the release of circulating natriuretic peptides in
teleost fish (Kaiya and Takei,
1996
; Smith et al.,
1991
; Westenfelder et al.,
1988
).
In the present study, no significant change in drinking rate was observed following intra-arterial administration of hypertonic mannitol and sucrose, suggesting the lack of a hypervolaemic effect on drinking in elasmobranchs. However, injection of hypertonic NaCl induced a significant decrease in drinking rate within 60 min of injection, which may suggest a specific but perhaps transient effect of NaCl on the drinking response of S. canicula.
The only natriuretic peptide in elasmobranchs appears to be C-type
natriuretic peptide (CNP) (Suzuki et al.,
1994; Kawakoshi et al.,
2001
), so it is reasonable to assume that CNP may act in
elasmobranchs in a manner similar to ANP in teleost fish. Recent
investigations using homologous CNP have demonstrated CNP inhibition of an
angiotensin-II-induced drinking response in S. canicula, and the dose
of CNP required to induce this anti-dipsogenesis was 50 times lower than the
dipsogenic dose required for angiotensin II
(Anderson et al., 2001a
).
However, intravascular administration of homologous CNP in A.
japonica had no effect on drinking rate
(Tsukada and Takei, 2001
), but
cerebral ventricular administration of CNP in mammals has been shown to induce
drinking (Samson et al.,
1991
).
Hypervolaemia is a potent stimulus for rectal gland secretion in
elasmobranchs (Solomon et al.,
1985) and is also considered to be the predominant stimulus for
CNP secretion into the circulation (Loretz
and Pollina, 2000
). Interestingly, the rectal gland acts as a
specific route of excretion of NaCl in elasmobranchs, and CNP is known to
stimulate rectal gland secretion in vitro in both S.
canicula and the spiny dogfish Squalus acanthias
(Solomon et al., 1992
;
Anderson et al., 1995
). It is
evident that the inhibitory mechanisms of drinking in both teleosts and
elasmobranchs are very complex and largely unknown. Clearly, the potential
action of hypervolaemia and, in particular, of the administration of
hypertonic NaCl on the drinking rate of elasmobranchs requires further
research and must be considered alongside the stimulatory role of CNP on
rectal gland function.
The present study has demonstrated that the increase in drinking rate in
elasmobranchs acclimating to increased environmental salinity appears to be
mediated by extracellular dehydration or hypovolaemia. Controlled haemorrhage
of 5.7% of blood volume caused a significant and immediate increase in
drinking rate in S. canicula. In mammals, an 8-10% deficit in
extracellular fluid volume is required to induce dipsogenesis
(Fitzsimons, 1998), and in
freshwater-acclimated A. japonica a reduction of as much as 30% of
total blood volume was required before drinking began
(Hirano, 1974
). It appears,
therefore, that S. canicula was particularly sensitive to a reduction
in blood volume. The increased drinking in the haemorrhaged S.
canicula was almost immediate in comparison with the delayed drinking
response observed in the fish presented with a salinity challenge. The delay
in the drinking response was probably due to a more gradual hypovolaemia as
the fish acclimated to the increased environmental salinity, indicating that a
threshold of extracellular fluid loss during acclimation to the hyperosmotic
environment of 100% SW may have to be reached prior to the initiation of
drinking.
Undoubtedly, passive movement of NaCl and water across the gill membranes
will occur as elasmobranchs acclimate to the more concentrated environment of
100% SW. This study is the first to demonstrate that a drinking response may
contribute to the observed independent increase in plasma Na+ and
Cl- concentrations during acclimation to increased environmental
salinities. The reduction in blood volume during acclimation to increased
environmental salinity, initiating a drinking response, is similar to the
response observed in teleost fish (Hirano,
1974; Takei et al.,
1988
), in which it appears that angiotensin II is the primary
modulator of the drinking response (Takei
et al., 1988
). Sequencing of homologous elasmobranch angiotensin I
(Takei et al., 1993
) and
subsequent identification of angiotensin-II-like receptors in T.
scyllia (Tierney et al.,
1997
) has indicated that angiotensin II may also play an important
role in elasmobranch osmoregulation. Kobayashi et al.
(1983
) reported a lack of
drinking in elasmobranch fish following administration of angiotensin II.
However, that study used a less-sensitive dye-dilution technique than that
used in the present study and may not have detected the low basal drinking
rates in seawater-acclimated elasmobranch fish reported in this and other
studies (Hazon et al.,
1999
).
Recent investigations have demonstrated a potent dipsogenic response to
homologous angiotensin I that can be blocked by the co-administration of the
angiotensin converting enzyme inhibitor captopril and, furthermore, both
S. canicula and T. scyllia responded to the administration
of homologous angiotensin II with a dose-dependent increase in drinking rate
(Anderson et al., 2001b). These
results, combined with the present study, indicate that the
reninangiotensin system may play an important role in the regulation of
drinking during acclimation to increased environmental salinities.
In summary, the present study has demonstrated a drinking mechanism in the more primitive marine elasmobranch fishes that were considered not to have the physiological requirement, indeed capacity, to drink for osmoregulatory purposes. This drinking response is initiated during acclimation to hyperosmotic environments and is triggered primarily by hypovolaemia in a manner similar to that described previously for teleost fish.
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Acknowledgments |
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