The effect of desiccation on water management and compartmentalisation in scorpions: the hepatopancreas as a water reservoir
Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel
* Author for correspondence (e-mail: gefene{at}unlv.nevada.edu)
Accepted 1 March 2005
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Summary |
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Key words: scorpion, water, desiccation, hepatopancreas, haemolymph, adaptation, osmoregulation
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Introduction |
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Both the behavioural (e.g. burrowing, nocturnal activity) and physiological
(e.g. highly impermeable integument) adaptations of scorpions to dry
conditions have been extensively studied (reviewed in
Hadley, 1990). Generally,
arthropods of xeric distribution have integuments more resistant to water loss
in comparison with more mesic species
(Edney, 1977
). In a number of
studies scorpions have been shown to follow this general rule
(Toye, 1970
;
Warburg et al., 1980
;
Robertson et al., 1982
), but
recent evidence suggests that previously reported interspecific differences in
water relations of scorpions may in fact be phylogenetically related
(Gefen and Ar, 2004
).
Rates of water loss to the environment have been recorded for a number of
species, but little is known about water compartmentalisation in scorpions.
Seasonal fluctuations of water distribution in several body compartments have
been reported (Warburg, 1986;
Warburg et al., 2002
), but
these are of limited contribution to the understanding of water management
during prolonged desiccation under controlled laboratory conditions. Moreover,
to the best of our knowledge, there are no reported measurements of haemolymph
volume for any scorpion species.
The haemolymph is the largest extracellular water reservoir of all land
arthropods, and often reduces in volume during dehydration. Insects lose water
primarily from the haemolymph during dehydration
(Edney, 1977;
Hyatt and Marshall, 1985
;
Naidu and Hattingh, 1986
;
Albaghdadi, 1987
;
Zachariassen and Pedersen,
2002
). By contrast, Greenaway and MacMillen
(1978
) reported that the
terrestrial crab Holthuisana transversa (Martens) loses water
proportionately from the haemolymph and a second compartment. Two other
species of land crabs Gecarcoidea lalandii and Cardisoma
carnifex maintained their haemolymph volume at the expense of tissue
water while dehydrated (Harris and
Kormanik, 1981
). Muscle tissue
(Horowitz, 1970
) and the gut
and hepatopancreas (Lindqvist and
Fitzgerald, 1976
) have been suggested as possible sources of water
in desiccating isopods. Hadley
(1994
) suggested that while the
developed tracheal system of insects allows them to tolerate large decreases
in haemolymph volume during dehydration, some spiders and crustaceans maintain
haemolymph volume in order to preserve its respiratory role.
Scorpions of the Family Buthidae were shown to be better haemolymph
osmoregulators and more desiccation resistant than their respective
Scorpionidae sympatric species (Gefen and
Ar, 2004). In addition, the haemolymph osmotic concentrations of
the buthids decreased following mild desiccation, suggesting water
mobilization from another body compartment to the haemolymph. We used the same
experimental design that was employed in the previous study
(Gefen and Ar, 2004
), where
Buthidae and Scorpionidae were each represented by both xeric and mesic
species/subspecies, in order to elucidate the physiological mechanisms
involved in the observed between-family differences in water relation traits.
We monitored body water management by following changes in the haemolymph,
hepatopancreas and total body water stores through a range of mass loss levels
under controlled desiccating conditions, in order to determine the role played
by the hepatopancreas in the water budget of desiccating scorpions. We also
measured the lipid content of the hepatopancreas in an attempt to examine the
contribution of oxidized metabolic fuels to the overall water budget of
scorpions under prolonged desiccation conditions.
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Materials and methods |
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Haemolymph osmolarity
Following capture, the scorpions were held in the laboratory at room
temperature in round (9 cm diameter) plastic boxes with soil from the
collection site, and fed adult crickets ad libitum for 14 days. The
boxes were perforated in order to allow gas exchange with ambient
atmosphere.
The scorpions were then weighed to the nearest 0.1 mg, and a sharpened
glass capillary was inserted into the pericardial sinus by puncturing the
dorsal intersegmental membrane. The haemolymph (10 µl) withdrawn was
used for determining its initial osmolarity (5100C Vapour Pressure Osmometer,
Wescor, Logan UT, USA). The tapered tip of the glass capillary enabled
immediate closure of the wound. Nevertheless, occasionally specimens had to be
excluded from further investigations when haemolymph withdrawal resulted in
persistent bleeding.
After allowing 24 h for recovery, the scorpions were weighed again, transferred to identical empty plastic boxes and randomly assigned to one of the experimental mass loss groups. The boxes were placed in a controlled temperature chamber (30±0.2°C, 40-60% RH). The animals and their excretions were weighed daily, and following losses of 5, 10, 15 or 20% of initial mass (excluding dry excretions) the haemolymph osmolarity of the scorpions was measured again.
Body water distribution
(1) Total body and hepatopancreas water contents
Following haemolymph sampling the scorpions were decapitated, and their
hepatopancreas was removed. Fresh mass of the hepatopancreas was measured to
the nearest 0.1 mg. Then the hepatopancreas and rest of the body were dried
separately at 60°C to constant mass. Whole body and hepatopancreas water
contents were calculated using the differences between wet and dry masses, and
expressed as a percentage of total body and hepatopancreas masses
respectively.
(2) Haemolymph volume
Additional scorpions were sampled for haemolymph volume, which was
determined in control (following 14 days of ad libitum feeding), and
in 10% and 20% mass loss experimental groups. Haemolymph volume was measured
using isotope dilution of [methoxy-3H]-inulin (specific activity:
380 mCi g-1; Perkin Elmer, Boston MA, USA). 5 µl (10±0.1
µl syringe, Hamilton, Bonaduz, Switzerland) of 3H-inulin
solution (30,000 cpm µl-1) were injected into the pericardial
sinus through the dorsal intersegmental membrane using a micromanipulator.
Dilution time was set to 75 min since preliminary experiments had shown no
changes in inulin concentrations between 60-90 min following injection.
Haemolymph was sampled after 75 min by withdrawing the syringe and collecting
haemolymph with a glass capillary. Its osmolarity was measured, and 8 µl
aliquots were placed in scintillation vials with 5 ml Optifluor liquid
scintillation fluid (Packard, Meriden CT, USA). Radioactivity was counted in a
liquid scintillation analyzer (Tri Carb 2100TR; Packard, Meriden, CT, USA).
Volume determination was carried out by comparing haemolymph radioactivity
levels to standards of known water volume injected with 5 µl of the
[methoxy-3H]-inulin solution.
Hepatopancreas lipid content
Dried hepatopancreas was used for determination of hepatopancreas lipid
content. The tissue was placed in emptied tea-bags, which were then stapled
shut, weighed to the nearest 0.1 mg and put in the extractor of a Soxhlet
apparatus, with petroleum ether as the extraction solvent. Samples were
extracted for 24 h, and then dried at 60°C to constant weight.
Hepatopancreas lipid content was determined by the difference in dry mass of
the samples before and after the lipid extraction, and expressed as a
percentage of the total hepatopancreas dry mass. No significant difference was
found between pairs of samples from the same hepatopancreas (Wilcoxon matched
pairs test, P=0.33; N=15).
Statistics
Statistical analysis was carried out using STATISTICA© 6.0
for Windows software. All data expressed as a percentage were arcsine
transformed prior to further statistical analysis. Newman-Keuls test was used
for posthoc comparisons. Total body mass was used as a covariate for ANCOVA.
Mass did not have a significant effect on transformed values
(P>0.25).
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Results |
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Differences in WLR of the four species have been reported previously
(Gefen and Ar, 2004), and can
also be inferred from the time interval until desiccation to a given level of
mass loss. For example, B. judaicus and L. quinquestriatus
(Buthidae) lost 10% of their initial mass after 18.6±5.2 (mean ±
S.D.) and 19.3±6.9 days, respectively, while the
two scorpionids lost mass twice as fast, losing 10% body mass after
9.4±5.0 and 8.6±2.9 days (for S. m. fuscus and S.
m. palmatus, respectively).
Body water distribution
(1) Total body and hepatopancreas water contents
Scorpion samples included both males and females and it was, therefore,
necessary to address possible differences between the sexes. The number of
male specimens was relatively low, and a statistical comparison within each
species and mass loss level would therefore have been of little meaning.
However, it is evident from Fig.
1 that water content values (percent of total mass) of male and
female scorpions are similar, allowing pooling male and female values within
each species.
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Fig. 2 shows the body water contents of the four species, expressed as a percentage of total body fresh mass, over the range of experimental mass loss levels. Initial water stores of the two Scorpionidae are higher, but only that of S. m. palmatus is statistically significant, in comparison with those of the Buthidae (ANCOVA, P<0.01). However, the body water stores of Buthidae are better maintained when the scorpions are exposed to desiccating experimental conditions. Despite their higher initial values, the water contents of Scorpionidae decrease rapidly, and are significantly lower than initial values after mass loss of only 5% (Fig. 2). By comparison, a statistically significant decrease in water contents of L. quinquestriatus is only seen at 20% mass loss, while B. judaicus kept body water content stable throughout the range of experimental mass loss levels.
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A similar pattern was recorded for depletion of water stored in the hepatopancreas (Fig. 3). As with total body water, both scorpionids appeared to have larger water stores in the hepatopancreas in comparison with buthids, although these differences were marginally short of the generally accepted significance level of 0.05 (e.g. for S. m. palmatus vs L. quinquestriatus P=0.053). Scorpionids also exhibited a significant decrease in hepatopancreas water stores after mass loss of 5%, while a similarly significant decrease was recorded in buthids only after loss of 20% of initial body mass (Fig. 3).
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The role of the hepatopancreas in the water budget of scorpions was further
assessed by calculation of the hepatopancreas water content as a fraction of
the total water content of the scorpion, following the same experimental
desiccation levels (Fig. 4). As
females generally have a larger hepatopancreas than males, and because of the
smaller number of captured males, this comparison was limited to females only.
L. quinquestriatus females stored significantly more water in the
hepatopancreas (expressed as fraction of total body water) in comparison with
the other three studied species [F(3,17)=3.52;
P=0.04]. In all examined species, the proportion of hepatopancreas
water to the total body water decreased significantly during prolonged
desiccation (regression of arcsine transformed percentages, =0.05), but
the steepest slope calculated was also that of the xeric buthid L.
quinquestriatus (Fig. 4).
This slope was not significantly different (t-test, P=0.21)
from that of the other buthid, B. judaicus, but was steeper in
comparison with the slopes for S. m. palmatus and S. m.
fuscus at significance levels of 0.05<P<0.1 and
P<0.05, respectively.
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(2) Haemolymph volume
Another contribution to the higher total water content of scorpionids comes
from their high haemolymph volume in comparison with that of buthids
(Table 2). The two scorpionids
had significantly higher ratios of haemolymph volume to total body mass than
L. quinquestriatus. The haemolymph volume fraction of S. m.
palmatus was also significantly higher than that of B. judaicus
(ANCOVA, P=0.05). None of the four species showed a significant
decrease in the ratio of haemolymph volume to total body mass following
desiccation to 10% loss of initial mass
(Table 2). Furthermore,
following desiccation of L. quinquestriatus to 10% loss from initial
body mass, the fraction of haemolymph volume to total body mass increased
significantly (Table 2, ANCOVA,
P<0.001). Haemolymph volume measurements of scorpionids following
20% mass loss was not possible due to the difficulty of withdrawing
haemolymph, thus suggesting a severe decrease in haemolymph volume at these
desiccation levels.
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Hepatopancreas lipid content
Lipid contents of the hepatopancreas, expressed as a percentage of tissue
dry mass, are given in Table 3
for the four species over the range of experimental mass loss levels. No
significant difference (P>0.05) is evident for either of the
Buthidae following losses of up to 20% of initial mass. By comparison, for
Scorpionidae there was a significant increase in hepatopancreas lipid fraction
as a result of desiccation. The most pronounced increase was that of S. m.
fuscus, which showed a significantly higher hepatopancreas lipid fraction
following loss of as little as 5% of its initial mass
(Table 3).
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Assessment of changes in the total lipid contents was hampered by the variability in body and hepatopancreas masses, together with the limited sample sizes. For example, initial body masses of S. m. fuscus were 2.124±0.254 g and 1.625±0.107 g (mean ± S.E.M.) for 5% and control mass loss groups, respectively. Nevertheless, the hepatopancreas lipid content of the 5% mass loss group was 249.7±38.4 mg (57.3% of total hepatopancreas dry mass of 435.7±63.4 mg; N=9, four males and five females), which constituted a significant increase in lipid content from control values (111.4±15.6 mg, 43.5% of 255.8±28.3 mg hepatopancreas dry mass; N=6, three males and three females), even when accounting for the evident difference in hepatopancreas dry mass (ANCOVA, P<0.05).
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Discussion |
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Initial WLR, measured during the early stages of desiccation, are
relatively high (Hadley, 1994;
Gefen and Ar, 2004
). Therefore,
the recorded desiccation time is not an accurate measure of steady-state WLR
of the four species, particularly at lower mass loss levels. Nevertheless, it
has been previously shown that osmoregulatory capacities of scorpions are
negatively correlated with WLR (Gefen and
Ar, 2004
). The haemolymph osmolarity of the millipede
Pachydesmus crassicutis was shown to increase more at high
dehydration rates (Woodring,
1974
). Likewise, interspecific differences in the osmoregulatory
capacities of terrestrial isopods were found to correlate well with their
position on a `terrestriality gradient' and their respective WLR
(Price and Holdich, 1980
).
It has been suggested that isopods mobilise water from a different body
compartment to the haemolymph upon desiccation
(Horowitz, 1970;
Lindqvist and Fitzgerald,
1976
). If the same mechanism occurs in scorpions, their ability to
osmoregulate their haemolymph may depend on the ratio of water mobilisation
rate from another body compartment
(
1) to the water loss rate
(WLR,
2). Thus, at a high
desiccation rate, when
2/
1
is relatively high, water supply cannot meet demand and haemolymph osmotic
concentration can not be maintained. By comparison, if
2/
1
is lower at lower desiccation rates, the regulation of haemolymph osmolarity
may be possible. However, while water vapour deficit across the integument
dictates continuous transpiratory water loss
(
2 remains steady),
depletion of body water stores (decreasing
1 as desiccation is
prolonged) means that osmoregulation may be restricted to a limited range of
water losses. Interestingly, the observed initial decrease in haemolymph
osmolarity following the onset of desiccation in buthids
(Gefen and Ar, 2004
) suggests
that water mobilisation from another compartment is not triggered by increased
haemolymph osmolarity.
The interrelated water loss and mobilisation rates and osmoregulatory
capacities are also consistent with the water depletion pattern shown in
Fig. 2. The significant
decrease in total body water stores of scorpionids following a mass loss of
only 5% from initial body mass is coupled with their relatively high WLR,
particularly during the early stages of desiccation. Similarly, the highest
drop in total body water stores was recorded for S. m. fuscus
(Fig. 2), which correlates well
with the species' highest WLR and poorest osmoregulatory capacity among the
four studied species (Table 1;
Gefen and Ar, 2004). By
contrast, the reported low WLR of buthids are reflected in the ability to
maintain body water and osmotic stability. These lower WLR allow metabolic
water production to compensate better for water loss to the environment, thus
minimising loss of initially stored bulk water during desiccation
(Gefen and Ar, 2004
).
The hepatopancreas is a large organ, which fills the entire mesosoma and
the first two metasomal somites of scorpions
(Warburg et al., 2002). The
similar depletion patterns of the hepatopancreas
(Fig. 3) and total body water
stores (Fig. 2) hint at the
important role played by the former in the overall water budget of the
desiccating scorpion. Furthermore, initially comprising
30% of the total
body water content of B. judaicus, S. m. fuscus and S. m.
palmatus, the fraction of hepatopancreas water from total body water
decreases during desiccation (Fig.
4). This suggests that the contribution of hepatopancreatic water
stores is higher than expected if water was to be proportionally lost from all
body compartments. The contribution of hepatopancreatic water to haemolymph
volume regulation (Table 2) is
therefore fundamental for maintaining osmotic stability of the haemolymph.
The role of the hepatopancreas in water management during desiccation is
even more pronounced in the case of the xeric buthid L.
quinquestriatus. Among the studied species, female L.
quinquestriatus store the highest amount of water in the hepatopancreas.
Furthermore, their significantly higher slope
(Fig. 4) indicates that female
L. quinquestriatus mobilise more water from the hepatopancreatic
stores during prolonged desiccation, with the hepatopancreas water content
reaching values similar to those of the other species after 20% loss of
initial mass (Fig. 4). The
significantly higher contribution of the hepatopancreatic water stores of
L. quinquestriatus to the total water loss may contribute to its
haemolymph osmotic stability. The ability of L. quinquestriatus to
osmoregulate its haemolymph during prolonged desiccation is similar to that of
B. judaicus, despite the higher WLR recorded for the former at
30°C (Gefen and Ar,
2004).
Mobilisation of hepatopancreatic water stores may contribute to volume
regulation of the haemolymph during desiccation. Unlike insects, scorpions
lack a tracheal system, and rely on haemolymph oxygen carriers for respiratory
gas exchange between their tissues and the surrounding environment through
their book lungs. It has been suggested that this respiratory role of the
haemolymph in some non-insect arthropods may explain the strategy of
regulating haemolymph volume at the expense of tissue water stores during
desiccation (Hadley, 1994).
Measurements of haemolymph volume (Table
2) and hepatopancreas water content
(Fig. 3) are in agreement with
this suggested pattern. None of the four examined species showed a decrease in
the fraction of haemolymph volume to total body mass of the scorpion following
desiccation to 10%. Furthermore, as total body water stores diminish during
desiccation (Fig. 2), the
fraction of haemolymph to total body water stores increases.
Mobilisation of water from hepatopancreatic stores to the haemolymph is
best shown for L. quinquestriatus, where the significantly highest
rate of hepatopancreas water depletion
(Fig. 4) is coupled with a
significant increase in the water fraction of the haemolymph from total body
mass (Table 2). However, we
have not managed to determine the origin of this characteristic of the xeric
L. quinquestriatus (Buthidae). The present study and a previous one
(Gefen and Ar, 2004) have shown
interspecific differences in water relations of scorpions to be primarily
phylogenetically related rather than mechanisms of adaptation to arid
habitats. Unfortunately, B. judaicus (Buthidae) specimens used for
haemolymph volume determination were kept under laboratory conditions longer
than the other species before measurements and, therefore, may not have
started desiccation at their fully hydrated state. Their initial haemolymph
osmolarity of 638±12 mOsm l-1 in comparison with
569±3 mOsm l-1 of fully hydrated B. judaicus
(Table 1) indicates that this
suggestion can not be ruled out.
The two Scorpio maurus subspecies regulated their haemolymph volume during mild desiccation, but their haemolymph volume could not be determined after loss of 20% of initial mass (Table 2). This severe level of desiccation made haemolymph withdrawal impossible, probably as a result of considerable haemolymph depletion. Fig. 3 shows that the water stored in the hepatopancreas of Scorpionidae is rapidly lost up to loss of 10% of initial body mass, whereas the relative volume of their haemolymph is maintained (Table 2). Following further desiccation, haemolymph volume may decline as demand for water cannot be met by the depleting hepatopancreatic stores (Fig. 3). It is worth noting that mortality rates among scorpionids following severe desiccation were much higher in comparison with buthids (E.G. and A.A., unpublished).
Terrestrial arthropods can survive desiccation stress through one or more
of three physiological mechanisms. These include (1) storage of large
quantities of water as bulk water or metabolic water; (2) reduced rates of
water loss to the environment; (3) the ability to tolerate the loss of
relatively large fraction of their initial body water stores
(Gibbs et al., 2003). When
pooling total body and hepatopancreas water contents of the two studied
scorpion families (Fig. 5), it
seems that they adopt different strategies in avoiding desiccation.
Scorpionids exhibit a rapid depletion of body water stores, which reflects
their higher WLR in comparison with those of buthids
(Gefen and Ar, 2004
), but
appear to store more bulk water in their bodies when fully hydrated
(Fig. 5). The changes in
hepatopancreas lipid content during desiccation also appear to be
phylogenetically related, with only the two Scorpionidae exhibiting a
significant increase in lipid fraction following desiccation
(Table 3). Glycogen water
binding capacity is estimated to be 3-5 times its own mass
(Schmidt-Nielsen, 1997
).
However, glycogen-bound water is only available to the organism as glycogen is
catabolised. Therefore, high WLR may necessitate glycogen catabolism not only
for meeting energetic needs and production of metabolic water, but also for
making bulk water available for maintaining homeostasis during prolonged
desiccation. This could be accompanied by lipogenesis from a carbohydrate
source, as has been suggested for several Drosophila species exposed
to desiccating conditions (Marron et al.,
2003
).
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In conclusion, we show that scorpions use the hepatopancreas as a water reservoir. Water is stored both as bulk water, and as potential metabolic water source in the form of metabolic fuels. The hepatopancreatic water stores are used to replenish lost haemolymph water upon desiccation, as haemolymph volume is regulated at the expense of other body stores. However, the contribution of hepatopancreatic water under the experimental conditions is sufficient for maintaining osmotic stability only when WLR are relatively low, as in the case of Buthidae. By contrast, the high WLR of Scorpionidae results in rapid depletion of body water stores and poor osmoregulatory capacities during desiccation.
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Acknowledgments |
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References |
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