Salt and water regulation by the leatherback sea turtle Dermochelys coriacea
1 School of Environmental Science, Engineering and Policy, Drexel
University, Philadelphia, PA 19104, USA
2 Department of Biological Sciences, Florida Atlantic University, Boca
Raton, FL 33431, USA
* e-mail: Richard.Reina{at}drexel.edu
Accepted 5 April 2002
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Summary |
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Key words: ion regulation, sodium, water balance, leatherback sea turtle, Dermochelys coriacea, osmoregulation, salt gland
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Introduction |
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Salt glands are all composed of specialised, secretory cells that
concentrate Na+ and Cl- from the blood to the lumen of
secretory tubules through an energy-dependent process
(Abel and Ellis, 1966;
Gerstberger and Gray, 1993
)
and drain at the corner of the eye, through the nostrils or on the surface of
the tongue. The biochemical processes through which ions are concentrated have
been extensively studied in birds (e.g.
Gerstberger and Gray, 1993
;
Shuttleworth and Hildebrandt,
1999
), but our understanding of reptilian salt glands has not yet
reached a similar level (Franklin et al.,
1996
; Reina and Cooper,
2000
; Shuttleworth and
Thompson, 1987
). However, chelonian salt glands certainly possess
the necessary cellular and vascular structures to support the requirements of
extensive energy-dependent ion transport
(Abel and Ellis, 1966
;
Ellis and Abel, 1964
).
Sea turtle lachrymal salt glands secrete a solution composed almost
entirely of sodium chloride at approximately 1500-1800 mosmoll-1
(Marshall and Cooper, 1988;
Nicolson and Lutz, 1989
;
Reina and Cooper, 2000
) in
response to increasing plasma Na+ concentration, and their activity
is regulated by microcirculatory changes in or near the glands
(Reina, 2000
). Both adrenergic
and cholinergic stimulation of the salt gland of the green turtle Chelonia
mydas stop secretion within 2 min and inhibit its activity for a
dose-dependent duration (Reina and Cooper,
2000
). Chelonian salt glands are not activated by either
adrenergic or cholinergic stimulation, unlike the typical antagonistic actions
of sympathetic and parasympathetic stimulation on avian salt glands
(Fänge et al., 1963
;
Lowy et al., 1989
). The
reasons for this phenomenon are unclear and require further investigation.
The leatherback turtle Dermochelys coriacea diverged
evolutionarily from other living sea turtles some 100 million years ago
(Pritchard, 1997) and
possesses many striking morphological and physiological differences such as
growth rate (Zug and Parham,
1996
), thermoregulation
(Paladino et al., 1990
) and
type of diet (Bjorndal, 1997
;
Eisenberg and Frazier, 1983
).
Leatherbacks subsist on a diet of jellyfish and other gelatinous invertebrate
prey that are approximately iso-osmotic with sea water and low in nutritional
value (Lutcavage and Lutz,
1986
). The large quantities of coelenterates required to support
the growth rate must result in an enormous salt load. However, the response of
the salt glands to a large salt load has never been measured in leatherbacks
of any age.
To reach the sand surface after hatching from the egg, hatchling turtles
must spend several days digging vertically through the sand and may lose over
10% of their hatched body mass (Bennett et
al., 1986). In addition to emerging from nests that are deeper
than those of other species (Billes and
Fretey, 2001
), leatherback hatchlings on some beaches must crawl
more than 100 m to reach the water. With deep nests, long crawls to the ocean
and an invertebrate diet, neonate leatherbacks are probably more osmotically
stressed than any other marine vertebrate. Their state of hydration and
osmoregulatory effectiveness are probably vital factors influencing their
ability to emerge from the nest, reach the ocean and survive. However, we know
nothing of the salt and water balance of leatherback hatchlings during these
important first few days of life. Previous studies of sea turtle salt gland
physiology have shown that salt glands are an essential route of extra-renal
salt secretion, but this study focuses on a quantification of water loss and
gain by neonates under the specific conditions that they encounter following
hatching from the egg. We hypothesised that neonate leatherbacks would
experience significant changes in salt and water balance during exposure to
sand and sea water and that they would osmoregulate effectively to reach
homeostasis. To test this hypothesis, we measured changes in mass, water and
Na+ concentration over time, determined the threshold for
activation of their salt glands, quantified the salt-secreting ability of
their salt glands and tested adrenergic and cholinergic control of salt gland
secretion.
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Materials and methods |
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Collection of samples
We collected and measured tear samples as described previously
(Marshall and Cooper, 1988;
Reina, 2000
;
Reina and Cooper, 2000
). Tear
samples from the corner of the eye were drawn into 5 µl micropipettes, and
we determined flow rate from the time taken to fill the tube. The contents of
the micropipettes were absorbed directly onto filter paper discs for immediate
measurement of total osmotic concentration (Wescor HR-33T dew-point
microvoltmeter), and the discs were then sealed in Eppendorf tubes for
subsequent analysis of sodium content by atomic absorption spectrophotometry.
We determined the mass-specific rate of tear production (ml kg-1
h-1) and tear Na+ concentration (mmoll-1)
from the right salt gland to calculate the mass-specific rate of removal of
Na+ by the gland (mmol Na+ kg-1
h-1). The technique does not easily permit simultaneous collection
from both salt glands but allows an accurate quantification of the output from
a single gland. Although the instantaneous rates differ between left and right
glands (Nicolson and Lutz,
1989
), we assumed that they balanced over the duration of the
experiment (Reina and Cooper,
2000
) so the rates of tear production and mass-specific
Na+ removal are presented for the whole animal with both glands
operating rather than for the right gland alone.
We took blood samples in insulin syringes (Terumo, 27Gx1/2) of
approximately 100 µl from the cervical sinus of hatchlings using the method
of Owens and Ruiz (1980). We
immediately transferred the blood to hematocrit tubes for centrifugation and
measurement of hematocrit. We then removed 5 µl of plasma and absorbed it
onto a paper filter disc for immediate measurement of blood osmotic
concentration as described above. The disc was then sealed for later analysis
of sodium content as described for the treatment of tear samples above.
We dissected and weighed salt glands from hatchlings that had not been exposed to sea water (N=5 animals) and from those that had been in sea water for 24h (N=5 animals). Animals were killed by chilling and freezing. We used the MannWhitney rank test to determine whether there was any difference in the mass of the salt glands before and after first exposure to sea water.
Experiments
We measured body mass, hematocrit and plasma Na+ concentration
of hatchlings over time immediately following their emergence from the nest.
Hatchlings did not eat during this time because they subsisted on internalised
yolk after hatching. We kept one group of animals (sibling turtles,
N=10) in a darkened box on damp sand for 12 h at 27 °C, then put
them into sea water at 27 °C for 12 h. We measured body mass and took
blood samples for measurement of hematocrit and plasma Na+
concentration at 0, 12 and 24 h. We maintained another group of animals
(sibling turtles, N=10) in sea water for 48 h, measured mass and
obtained blood samples at 0 and 48 h. We compared mass, hematocrit
(arcsine-transformed) and plasma Na+ concentration over time using
a repeated-measures analysis of variance (ANOVA) or non-parametric
MannWhitney rank test as appropriate
(Sokal and Rohlf, 1981).
We determined the secretory threshold in a dose/response manner by
injecting hatchlings turtles that had been exposed to sea water for 12 h with
salt loads of 0, 2, 4, 5 or 6 mmol NaCl kg-1 (25 ml
kg-1, N=6 each group) into the body cavity
(Reina and Cooper, 2000). If
visible salt gland secretion occurred within 40 min, we took a blood sample
and measured plasma Na+ concentration.
We quantified the secretory response of the salt gland by injecting animals (kept in sea water for 12 h) with a salt load of 27 mmol NaCl kg-1 (1.5 mol l-1 NaCl, 18 ml kg-1) into the body cavity and measuring the time elapsed to commencement of secretion. Phosphate-buffered saline (20 mmol l-1 NaH2PO4, 154 mmol l-1 NaCl, pH 7.2) was the volumetric control (2.7 mmol NaCl kg-1, N=6). We measured the flow rate, osmotic concentration and Na+ concentration of tears every 10 min for 80 min for newly hatched (N=6) and 4-day-old turtles kept in sea water (N=6). We compared the secretory responses of the two groups using the MannWhitney rank test. We measured secretion of the salt gland from commencement of secretion until cessation following a salt load of 13.5 mmol kg-1 (N=6), collected secretions every 30 min and took a blood sample when secretion stopped. A salt load of 13.5 mmol kg-1 was used to reduce the duration of the experiment and the possibility of dehydration changing the secretory response of the animals.
We examined the ability of the cholinergic agonist methacholine
(acetyl-ß-methylcholine chloride, Sigma) and of adrenaline (adrenaline
bitartrate, Sigma) to inhibit or stimulate secretion of the leatherback salt
gland in a manner similar to that previously shown in the green turtle
Chelonia mydas (Reina and Cooper,
2000). Methacholine was employed as an exogenous cholinergic
agonist because it is more resistant than acetylcholine to degradation by
cholinesterases (Cooper et al.,
1991
). We injected methacholine (10 ng kg-1, 100 ng
kg-1, 1 µg kg-1, 100 µg kg-1, 1 mg
kg-1 and 10 mg kg-1, N=6 for all groups) or
adrenaline (1 µg kg-1, 10 µg kg-1 and 1 mg
kg-1, N=6 for all groups) into the body cavity of animals
under three different experimental conditions. We examined the effects of
methacholine and adrenaline on (i) non-secreting animals to determine whether
the neurochemicals activated secretion, (ii) animals stimulated to secrete by
injection of a salt load of 27 mmol NaCl kg-1 to determine whether
they inhibited the secreting gland, and the effect of methacholine on
non-secreting animals when a subthreshold salt load was administered
simultaneously. We determined subthreshold salt load from the results of the
dose/response experiment described above. All hatchlings were kept in sea
water for 12 h before the experiments.
Statistical analyses
We used a MannWhitney rank test
(Sokal and Rohlf, 1981) to
determine significant differences in salt gland secretion rate among groups.
The program Statview v5.01 (SAS Institute) was used to conduct all statistical
tests. Significance was assumed at P<0.05, and all results are
shown as the mean ±1 S.E.M.
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Results |
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Salt gland mass before and after exposure to sea water
There was no significant difference between absolute or relative salt gland
mass of turtles exposed to sea water for 12 h (mass of both glands
109.0±5.3 mg, 0.33 % of body mass, N=5) or newly emerged
hatchlings that had not been exposed to sea water (mass of both glands
120.6±10.4 mg, 0.35 % of body mass, N=5). There were no
visible differences in salt gland color or gross appearance between the
groups.
Secretory threshold
Salt glands of animals injected with 0, 2 and 4 mmol NaCl kg-1
did not secrete, four of six turtles secreted after a salt load of 5 mmol NaCl
kg-1 and all turtles secreted after a salt load of 6 mmol NaCl
kg-1 (N=6 all groups). At the time secretion commenced,
plasma Na+ concentration was 214±8 mmol l-1
(N=6), significantly higher than that of untreated animals
(166.2±11.2 mmol l-1, N=6,
P<0.001).
Difference between day 0 and day 4 hatchlings in secretory
ability
Newly emerged turtles began secreting 16.3±2.1 min after being
salt-loaded with 27 mmol NaCl kg-1, significantly later than
4-day-old hatchlings, which began secreting after 10.3±1.1 min
(P<0.05). There were no significant differences in the rate of
tear production, tear Na+ concentration or total rate of
Na+ secretion by newly hatched and 4-day-old hatchlings
(Table 3). None of the newly
emerged (N=6) or 4-day-old hatchlings (N=6) secreted
following injection of an equal volume of phosphate-buffered saline. Data from
both age groups were pooled to determine the parameters of secretion because
there were no significant differences between them. When secretion was
initiated by salt loading, it reached 70 % of maximum rate in 2 min and peaked
at 4.84±0.52 mmol Na+ kg-1 h-1
approximately 20 min later (Fig.
1). At the termination of the experiment after 80 min of
secretion, the rate had fallen to 70 % of maximum. Approximately 20 % of the
injected salt load was removed in the first hour of secretion.
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Composition of secretions
The osmolarity of secreted tears of hatchlings was 1780±31 mosmol
l-1 (N=120), with 48.6 % of the osmolarity composed of
Na+ (865±25 mmol l-1).
Duration of the secretory response
Hatchlings that were injected with a salt load of 13.5 mmol kg-1
(N=5) secreted at a rate of 3.67±0.27 mmol Na+
kg-1 h-1 and stopped after 79.3±2.8 min, with
35.8±2.5 % of the injected salt load having been secreted. Plasma
Na+ concentration (190±16 mmol l-1) was
significantly higher than that in untreated animals (166.2±11.2 mmol
l-1, N=6, P<0.01) when secretion ceased.
Drug effects
Adrenaline did not stimulate the salt gland to secrete at any of the doses
examined (N=6 for all groups). Adrenaline did not affect the active
salt gland at a dose of 1 µg kg-1 but was a potent inhibitor of
secretion when administered at a dose of 1 mg kg-1, stopping
secretion within 2 min (Fig.
2). There appeared to be a dose-dependent response, with 10 µg
kg-1 adrenaline reducing but not abolishing secretion within 10 min
of injection (Fig. 2).
|
Methacholine also inhibited secretion from the active salt gland in a dose-dependent manner, with a dose of 10 mg kg-1 (N=6) inhibiting secretion within 2 min of injection and the inhibition continuing for up to 110 min (Fig. 3). At a dose of 1 mg kg-1 (N=6), methacholine significantly reduced the secretory output of the active salt gland within 10 min of injection, with maximum inhibition reached 20 min after injection. Secretion returned to the pre-treatment rate 30 min later (Fig. 3). The doses examined below 1 mg kg-1 had no effect. Methacholine alone did not visibly affect the inactive salt gland at any of the doses tested (N=6 for all groups). However, when simultaneously injected with a subthreshold salt load of 2 mmol NaCl kg-1 (determined from the results of the secretory threshold experiment described above), 100 µg kg-1 methacholine caused a transient secretion from the salt glands in six of eight of hatchlings. Secretory rate could not be determined from three of the secreting animals because secretion stopped before the collection pipette was filled, but for the remaining three animals the mean secretory rate was 0.40±0.2 mmol Na+ kg-1 h-1, significantly lower than the typical secretion rate measured from salt-loaded animals. The low rate was due to a reduction both in tear flow rate and in tear concentration, and the maximum duration of secretion was 10 min. This transient secretion was not seen at any of the other doses tested with the subthreshold salt load (100 ng kg-1, 1 µg kg-1, 50 µg kg-1, 1 mg kg-1 and 10 mg kg-1, N=6 for all groups).
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Discussion |
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Hatchlings without access to water lost approximately 5 % of their body
mass in just 12h, while they tolerated an increase in plasma Na+
concentration of over 20 % and an increase in hematocrit of approximately 27
%. Although the mass change in 12h was not significant, the changes in
hematocrit and plasma Na+ concentration suggest that water was
lost, resulting in their blood becoming more concentrated. It seems likely
that a significant mass loss would have occurred from dehydration if the
experiment had continued without access to water. The total extracellular
fluid volume (both plasma and interstitial) in a 38.2 g hatchling must have
been approximately 6 ml if the loss of 1.6 g mass as water resulted in an
increase in hematocrit of 27 %. The extracellular fluid (ECF) volume
calculated from mass and hematocrit changes was therefore approximately 16 %,
matching that determined empirically by Thorson
(1968) in a number of other
sea turtle species.
Hatchling turtles subsist on internalised yolk during the first few days of
life, and metabolism of this yolk results in the liberation of 90 % of its
mass as pre-formed and metabolic water
(Schmidt-Nielsen, 1990). This
liberated water helps to replenish some water lost through other routes, but
the remaining 10 % of yolk mass is consumed as energy and results in a net
loss of body mass in addition to that lost by dehydration. In terms of the
response of neonate leatherbacks to the environmental challenge following
hatching, the data show that, because neonates cannot drink in the desiccating
environment of the nest, their internal salt and water balances change
significantly. The hatchlings tolerate a loss of body water and increase in
plasma Na+ concentration rather than mobilising water stored in
internalised yolk, thereby preserving that vital energy reserve for the
energetic demands of digging, crawling and swimming.
Leatherback hatchlings lost body mass at a higher rate than loggerhead
(Caretta caretta) hatchlings exposed to similar conditions
(Bennett et al., 1986), but
unlike the loggerheads did not continue to lose mass on exposure to sea water.
They instead regained all lost body mass in 12h through drinking, with
approximately one-third (0.5 ml) of the consumed water entering the ECF,
assuming the ECF volume of 16 % of body mass calculated above and no change in
the number of red blood cells. The remaining water presumably remained in the
gut. The salt glands must have been actively secreting the consumed salt load
because there was no increase in plasma Na+ concentration during
the 12h in sea water.
Drinking sea water is an extremely effective osmoregulatory strategy used
by hatchling leatherbacks to offset the desiccation they experience during
emergence from the nest and exposure to air while crawling to the sea. Not
only can they regain lost body mass, but they are able to gain mass by
continuing to drink water while actively swimming and consuming their yolk
energy reserves. Hatchlings unrestrained in sea water for 48h increased in
body mass by 12 %. Plasma Na+ concentration was significantly
higher in all turtles kept in sea water than in newly hatched turtles and did
not return to the post-hatching concentration in the first 4 days. The data of
Bennett et al. (1986) show that
loggerhead hatchlings increased their plasma Na+ concentration to
140 mmoll-1 almost immediately after entering sea water, compared
with 120 mmoll-1 at emergence from the nest, and that the
concentration did not fall in the following 2 weeks in sea water. A mechanism
by which the effects of dehydration can be offset by sea turtles is to hatch
from the egg with a dilute plasma and to reach a new steady-state plasma
Na+ concentration after their first exposure to sea water.
Increased hydration at the time of emergence from the nest is correlated with
an increased survival time and improved physiological performance in the
snapping turtle Chelydra serpentina
(Finkler, 1999
). The data from
our study and that of Bennett et al.
(1986
) are consistent with this
strategy. On long-term exposure to fresh water, both hatchling green turtles
(Holmes and McBean, 1964
) and
diamondback terrapins Malaclemys terrapin
(Dunson, 1970
) had steady-state
plasma Na+ concentrations significantly lower than their seawater
counterparts, so turtles clearly have some plasticity in plasma ionic
composition.
Free water obtained from metabolism of the internal yolk supply can be used
to excrete Na+ from the salt glands as plasma concentration
increases with dehydration, but less energy would be required to retain this
metabolic water within the body to delay the concentration of plasma over time
when coupled with a lower initial plasma Na+ concentration. The
plasma Na+ concentration of leatherback hatchlings in sea water was
approximately 15-20 mmoll-1 higher than reported for other species
(Bennett et al., 1986;
Lutz, 1997
;
Reina and Cooper, 2000
); this
may be related to the enormous quantities of gelatinous prey that leatherbacks
must eat to fuel their rapid growth rate. Neonates must have a massive dietary
salt load because they need to eat approximately their own body mass in
coelenterates each day (Lutcavage and
Lutz, 1986
) so, by maintaining a higher plasma concentration, they
reduce the initial work required to maintain homeostasis. Previous studies had
not shown that neonate turtles use such a suite of mechanisms to survive the
challenges of hatching. By allowing their internal composition to change and
then establishing a new homeostatic state when able to drink, neonates
maximise the energetic resources available for escaping from the hatching
beach.
Leatherback hatchlings emerged from the nest fully prepared to osmoregulate
and showed no difference in salt gland mass or performance whether they had
been previously exposed to sea water or not. Unexposed turtles took
approximately 6 min longer to activate the gland but, once secretion began,
they secreted the same amount of salt as previously exposed turtles
(4.15±0.4 mmol Na+ kg-1 h-1), and both
groups reached maximum secretory rate approximately 20 min after secretion
commenced. We suggest that the 6 min difference between the two groups is due
to a priming of the stimulus/secretion pathway for first use of the salt
glands but that once it had occurred they were identical in all functional
respects. The tear concentration of hatchlings after salt loading was
approximately twice that of sea water and higher than previously reported for
this species (Hudson and Lutz,
1986) but similar to that of other sea turtle species studied
under similar conditions (Marshall and
Cooper, 1988
; Nicolson and
Lutz, 1989
; Reina and Cooper,
2000
). The total mass-specific secretory rate was slightly lower
than that reported for green turtle hatchlings of the same age
(Reina and Cooper, 2000
)
because the mass-specific flow of tears was slower per unit time.
Hudson and Lutz (1986)
measured spontaneous secretion in young juvenile unfed leatherbacks of
approximately half the osmotic concentration reported here, while fed animals
secreted at a concentration similar to that in the present study. The
spontaneous secretions almost certainly did not represent the true
osmoregulatory capacity of the turtles, but salt loading, either
experimentally or through the diet, results in the salt glands secreting at
maximum Na+ concentration. We measured a low Na+
concentration of 285±29 mmoll-1 in spontaneous secretions
from nesting adult females (N=5, data not shown). Nesting adult green
turtles also produce dilute salt gland secretions (P. Cooper, personal
communication). These results and the presence of mucocytes lining the canals
of sea turtle salt glands (Ellis and Abel,
1964
) strongly suggest a dual role for salt glands not previously
proposed. The tears of nesting adult females cannot serve an osmoregulatory
function because their formation will result in a net water loss. We propose
that the earliest hypothesis attributing a lubricative function to these tears
was correct (Carr, 1952
),
although later rejected (Schmidt-Nielsen
and Fänge, 1958
). We also propose that the salt gland is
capable of performing both a lubricative function with the mucocytes and an
osmoregulatory function when the principal secretory cells become active, as
determined by the homeostatic requirements of the animal at the time.
The threshold salt load required to initiate secretion was between 5 and 6
mmol NaCl kg-1, the same as that reported for hatchling
(Reina and Cooper, 2000) and
juvenile (Nicolson and Lutz,
1989
) green turtles. This amount of salt would be consumed in less
than 500 µl of sea water and resulted in an increase in plasma
Na+ concentration of 50 mmoll-1 by the time secretion
commenced. A greater salt load of 13.5 mmol NaCl kg-1 resulted in a
sustained salt gland secretion that stopped after approximately 80 min when
plasma Na+ concentration had fallen to 190 mmoll-1 but
was still significantly higher than in untreated animals. Animals injected
with 13.5 mmol NaCl kg-1 secreted a lesser proportion of the salt
load in the first hour than animals injected with 27 mmol NaCl kg-1
because of a lower mean secretory rate, but the Na+ concentrations
of the tears were not different. The lower mean secretory rate was a result of
the tailing off of Na+ secretion that occurs over time as salt is
removed, but the two groups secreted an approximately equal proportion of the
salt load over the first 30 min. Secretion stopped when less than half of the
salt load had been secreted, but the remaining salt in the body could not be
removed via the kidney without net water loss because of the
concentration of urine and its relative contribution to total Na+
efflux (Kooistra and Evans,
1976
). It seems likely that the salt glands recommenced secretion
subsequently, but this was not observed because the animals had since been
returned to the seawater holding tank. Measuring the secretion of animals over
a longer period following salt loading is problematic because the results of
this study show that hatchlings desiccate rapidly when not able to drink, and
it will therefore be difficult to isolate the animal's response to the salt
load from its response to desiccation.
Exogenous adrenaline and methacholine both had the same inhibitory action
on the hatchling leatherback salt gland as on the hatchling green turtle salt
gland (Reina and Cooper, 2000)
and inhibited the active gland with a delay and for a duration dependent on
dose. Systemic injection of methacholine stimulates the salt glands of the
crocodiles Crocodilus porosus and C. acutus
(Taplin et al., 1982
), the
diamondback terrapin Malaclemys terrapin
(Dunson, 1970
) and the herring
gull Larus argentatus (Fänge
et al., 1958
) within the range of doses examined in the present
study. It is perplexing why there is such a clear inhibitory action in the sea
turtles so far examined when dose and route of administration are the same as
in other reports. Neither adrenaline nor methacholine stimulated the salt
glands to secrete when injected alone, but an intriguing possibility is
suggested by the result that a low dose of methacholine (100 µg
kg-1) initiated a transient secretion when injected with a
subthreshold salt load of 2 mmol NaCl kg-1 in six out of eight
animals. Animals that were injected with the subthreshold salt load alone did
not secrete.
We propose that the sea turtle salt gland is downregulated unless Na+ concentration in the plasma or in some other compartment is elevated above a threshold that requires secretion to maintain homeostasis. If Na+ concentration is below the threshold at which secretion is inhibited, exogenous stimulation will not result in secretion because the gland is immediately inhibited endogenously in the absence of a need to secrete. Exogenous cholinergic stimulation concurrent with an elevation of Na+ concentration by a subthreshold salt load satisfies the two conditions required for secretion to begin but, because the amount of salt injected is small and hence Na+ concentration is elevated only slightly, the secretion is brief. Downregulation of the chelonian salt gland seems to be a plausible control mechanism because the huge osmoregulatory challenge faced by sea turtles will require the salt gland to function for a large proportion of the time.
Applying the estimates of Lutcavage and Lutz
(1986) of the mass of
jellyfish required daily by leatherback hatchlings and the secretory rate
measured in the present study, dietary salt consumption will exceed the
capacity of the salt glands to remove it. However, leatherback turtles possess
special structures in the esophagus and stomach to squeeze water from their
food items and to expel it from the mouth and nostrils, thereby reducing their
intake of salt and water from their prey. It is therefore difficult to
estimate their total Na+ intake, but it seems likely that it is of
a magnitude that requires almost constant secretion by the salt glands to
maintain internal ionic balance. Thus, a system of downregulation would be
efficient because it would only be required to inhibit intermittently when
salt secretion is not required; in contrast, a stimulatory system would need
to stimulate gland activity during the much larger proportion of the time that
the glands are active.
A similar dietary salt load is encountered by other species of marine
turtles; marine birds eat prey of lower salt content and therefore require
less salt gland activity to remove excess salt. This downregulatory system as
a consequence of dietary salt load may explain the different responses to
exogenous cholinergic stimulation in marine turtles and marine birds. However,
we are unlikely to elucidate more fully the salt gland control mechanisms
without in vitro techniques such as those used by Silva et al.
(1987,
1990
,
1993
) to isolate secretory
cells of the elasmobranch rectal salt gland from endogenous inhibition and
stimulation. Using cell culture techniques, we may be able to demonstrate
changes in ion-transport activity of chelonian salt gland cells in the
presence of exogenous modifiers.
This study showed that neonate leatherbacks tolerate the desiccating conditions of the nest by shifting their internal salt and water balances and that they are capable of re-establishing homeostasis once they encounter sea water. They use highly efficient salt-secreting glands that quickly activate after relatively small salt loads and that function intermittently as required. The control mechanism appears to inhibit the activity of the gland when secretion is not required, but the precise role of cholinergic nerves in the glands remains somewhat unclear.
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Acknowledgments |
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References |
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