Transport mechanisms of diuresis in Malpighian tubules of insects
Department of Biomedical Sciences, VRT 8004, Cornell University, Ithaca, NY 14853, USA
(e-mail: kwb1{at}cornell.edu)
Accepted 18 July 2003
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Summary |
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Key words: yellow fever mosquito, Aedes aegypti, Malpighian tubules, diuresis, diuretic peptide, kinin, leucokinin, intracellular cAMP, intracellular Ca2+, epithelial Na+ channel, Na+/K+/2Cl- cotransport, septate junction, paracellular Cl- conductance
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Introduction |
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Organs of salt and water balance |
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The primary organ of salt and water balance can change during metamorphosis
as, for example, in insects passing from aquatic to terrestrial habitats.
Mosquito larvae residing in freshwater use Malpighian tubules and the anal
papillae to maintain hemolymph volume and composition
(Bradley, 1987). Whatever
osmoregulatory function the larval gill may have had in freshwater is lost
with the transition to the air-breathing pupae. From here on, the Malpighian
tubules, salivary glands, midgut and hindgut are the major organs of salt and
water balance.
Larval Malpighian tubules serve to excrete the osmotic water loads in
freshwater. Initially, the blind-ended (distal) segment of the Malpighian
tubule secretes ions and some organic solutes, such as metabolic wastes and
substances foreign to the body, into the tubule lumen. Water follows solutes
by osmosis, increasing the hydrostatic pressure in the tubule lumen, which, in
turn, drives flow downstream to the proximal segment of the tubule and to the
gut. Along the way, solute, but not water, is reabsorbed, leaving behind a
dilute fluid that is excreted from the rectum. Thus, the water gained by
osmosis in freshwater is returned to the external environment, and the larval
mosquito remains in osmotic steady state even though its hemolymph is
hyperosmotic to freshwater by more than 300 mOsmol kg-1
H2O. When the external salinity increases above the osmotic
pressure of the hemolymph, insect larvae may increase the hemolymph
concentrations of proline and trehalose, thereby increasing hemolymph osmotic
pressure and minimizing osmotic water loss
(Patrick and Bradley,
2000).
Upon eclosion and flight into the desiccating terrestrial habitat, water
balance in the mosquito must switch from water excretion to water
conservation. From now on, Malpighian tubules must eliminate excess solute,
wastes and toxins with a minimum loss of water. Nevertheless, the tubules may
occasionally be called upon to secrete electrolytes and water at high rates,
responding to the large loads of gorging meals
(Maddrell, 1991).
Hematophagous (blood-feeding) insects, such as the blowfly Rhodnius
prolixus, can go for weeks without a meal, but, having found a source of
blood, the blowfly can take on a volume more than 12 times its own body mass.
The huge meal presents an enormous payload to a flying animal and also
challenges the osmotic and ionic balance of the hemolymph. To deal with both
threats, hematophagous insects quickly start a diuresis (increased urinary
excretion) that rids the animal of the unwanted salt and water fraction of the
blood meal (Adams, 1999
;
Williams et al., 1983
). In the
case of the yellow fever mosquito Aedes aegypti, only the female
feeds on blood and apparently only in association with the reproductive cycle.
From her perspective, she taps a convenient source of nutrients, vitamins,
minerals and electrolytes for her developing eggs
(Beyenbach and Petzel, 1987
).
From our perspective, she adds insult to injury; so prompt is the diuresis
that she begins to urinate even before she has completed her meal.
Even though there are some 14 000 species of hematophagous insects, rapid
and potent diuretic mechanisms may be more widespread than generally believed
(Adams, 1999). For example, the
glassy winged sharpshooter Homalodisca coagulata gorges on the sap of
oleanders, grapes and citrus fruit, causing great economic loss in California.
Like the blood-feeding yellow fever mosquito, the sharpshooter urinates while
feeding. Not that the ability to drink and urinate at the same time is
particularly dexterous, but the speed of processing the meal and excreting
unwanted solutes and water is nothing short of astounding
(Williams et al., 1983
).
Obviously, gorging insects in general, whether hematophagous or phytophagous,
must possess powerful epithelial transport systems.
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Renal turnover of the extracellular fluid compartment |
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In Malpighian tubules of insects, tubular secretion is the only mechanism
for presenting solute and water to the tubule lumen, as there is no glomerular
filtration. The renal turnover of the extracellular fluid compartment in
insects is therefore accomplished by the epithelial transport mechanisms of
secretion and absorption. Typically, the blind-ended, distal segment of the
Malpighian tubule secretes electrolytes, organic solutes and water, and
proximal segments further downstream reabsorb solute and water
(Beyenbach, 1995;
Linton and O'Donnell, 2000
;
Marshall et al., 1993
;
O'Donnell and Maddrell, 1995
;
Van Kerkhove, 1994
).
Reabsorption continues in the hindgut and rectum
(Chao et al., 1989
;
Coast, 2001
;
Phillips et al., 1996
;
Spring and Albarwani,
1993
).
In the yellow fever mosquito, Malpighian tubules of the female are much
larger than those of the male (Plawner et
al., 1991). The sexual dimorphism of the Malpighian tubules
reflects the capacity of the female to secrete the large salt and water loads
of the blood meal. Indeed, female Malpighian tubules secrete fluid in
vitro at a rate of 0.64 nl min-1 under control conditions;
male Malpighian tubules secrete at only 0.09 nl min-1. If fluid
secretion rates measured in vitro are similar to those in
vivo, then the five Malpighian tubules in the female yellow fever
mosquito secrete fluid at a rate of 3.2 nl min-1, or 4.6 µl
day-1, which must be completely reabsorbed further downstream. The
ejection of urine droplets from the rectum is so rare in the mosquito under
normal conditions that waiting for these droplets seems longer than waiting
for Godot. Since the hemolymph volume is 0.39 µl and the tubular secretion
rate is 4.6 µl day-1, it follows that, under control conditions,
Malpighian tubules turnover the hemolymph volume approximately 12 times per
day. The turnover rate is similar to that in warm-blooded mammals
(Table 1). However, under peak
diuretic conditions triggered by the blood meal, the turnover rate increases
more than 15-fold, processing the extracellular fluid volume 200 times per
day, which is beyond the capacity of the mammalian kidney
(Table 1). In a display of
renal bravura, urine droplets are now ejected from the rectum of the mosquito
in quick succession, approaching a flow rate of 60 nl min-1
(Wheelock et al., 1988
;
Williams et al., 1983
). Such a
high rate of diuresis is equivalent to voiding the entire hemolymph volume in
only 6.5 min. It would take 112 min for the two human kidneys to filter the
extracellular fluid volume. The comparison puts in perspective the power of
epithelial transport in Malpighian tubules when compared with filtration
systems.
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As the blood meal is in progress, the first droplets to be expelled from
the rectum are rich in NaCl. They rid the mosquito of the unwanted NaCl and
water, i.e. the plasma fraction of the blood meal. With time, Na+
excretion falls and K+ excretion rises, reflecting the intestinal
uptake of K+ after ingested red blood cells have been digested
(Williams et al., 1983).
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Active and passive transport |
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|
Transepithelial electrochemical potentials in Malpighian tubules of the
yellow fever mosquito show that Na+ and K+ are secreted
into the tubule lumen by active transport and Cl- is secreted by
passive transport (Williams and Beyenbach,
1984). As NaCl and KCl are secreted into the tubule lumen, water
follows by osmosis at a rate of 0.4 nl min-1, all under control
conditions in Malpighian tubules isolated from female mosquitoes fed on a diet
of 3% sucrose (Fig. 1C). The
rate of fluid secretion increases dramatically with or without changes in the
composition of secreted fluid consequent to stimulation with diuretic
peptides.
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The basic transepithelial transport system |
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|
|
Fig. 3 illustrates the basic transepithelial transport system under control conditions in Malpighian tubules of the yellow fever mosquito. There are two pathways into the tubule lumen: a transcellular pathway through principal and stellate cells and a paracellular pathway between these cells. Transcellular transport involves solute entry from the peritubular medium into the cell across the basolateral membrane, movement through the cell interior and exit across the apical membrane into the tubule lumen. The paracellular pathway bypasses epithelial cells. It is a direct route from the hemolymph to the tubule lumen through septate junctions located between epithelial cells.
Principal cells mediate the active transport for secreting Na+
and K+ into the tubule lumen
(Fig. 3A,B). The active
transport step is located at the apical plasma membrane of the brush border,
which is densely populated by an ATP-consuming proton pump, the V-type
H+-ATPase (Beyenbach,
2001). Originally found in vacuolar membranes of plants and
animals, the V-type H+-ATPase has now been found in the plasma
membrane of cells in invertebrates and vertebrates
(Harvey et al., 1998
). As
shown in Fig. 3C, the pump
consists of two major complexes, a cytoplasmic V1 complex capable
of catalyzing the hydrolysis of ATP, and a membrane-spanning V0
complex with the properties of a H+ channel
(Muller and Gruber, 2003
). The
reversible disassembly of the two complexes is thought of as one mechanism for
regulating pump transport activity
(Wieczorek et al., 2000
).
Protons secreted into the extracellular microenvironment of the brush
border are thought to return to the cell in exchange for Na+ and
K+, but it is unclear whether a single antiporter accepts both
cations or whether separate Na+/H+ and
K+/H+ antiporters are involved
(Fig. 3A). If antiport is
electrically neutral, exchanging one H+ ion for one Na+
or K+ ion, voltage is not a driving force
(Petzel, 2000). Therefore,
only the net concentration difference of H+ and Na+ (or
K+) across the plasma membrane determines the direction and
magnitude of the exchange transport. If the antiporter transports two
H+ ions for each Na+ (or K+) ion, then
voltage is an additional driving force
(Petzel et al., 1999
). In this
case, an apical membrane voltage of 120 mV (cell-negative) is able to drive
Na+ and K+ into the tubule lumen against a 100-fold
concentration difference.
The V-type H+-ATPase is likely to have an electromotive force larger than 146.1 mV, the electromotive force estimated for the apical membrane (Ea) in principal cells of Aedes Malpighian tubules (Fig. 3B). The high electromotive force gives rise to large voltages across the apical membrane (Va), on average 110.6 mV. Since the proton pump extrudes H+ from the cell without balancing charge, the transport of H+ constitutes current that must return to the cytoplasmic face of the pump. As shown in Fig. 3B, pump current returns to the pump by passing through conductive pathways located in the septate junction and the basolateral membrane. Positive current passing through the septate junction from the tubule lumen to the hemolymph is equivalent to that carried by Cl- passing from hemolymph to lumen, which is the mechanism of transepithelial Cl- secretion (Fig. 3A,B). Positive current passing across the basolateral membrane is carried largely by K+, which is the major mechanism for bringing K+ into the cell from the hemolymph (Fig. 3A). One consequence of the intraepithelial current loop formed by active and passive transport pathways is that one Cl- ion is secreted for every cation secreted into the tubule lumen. As a result, the sum of transepithelial Na+ and K+ secretion more or less equals the rate of transepithelial Cl- secretion (Fig. 1C; Tables 2, 3). Furthermore, the electrical coupling of active transcellular and passive paracellular transport pathways preserves electroneutrality of the solutions on both sides of the epithelium in spite of high rates of transepithelial salt and water flow.
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The absence of measurable ouabain-sensitive
Na+/K+-ATPase activity in Aedes Malpighian
tubules and the substantial inhibition of total ATPase activity with
bafilomycin, an inhibitor of the V-type H+-ATPase, suggest that
transepithelial transport is powered exclusively by the proton pump
(Beyenbach, 2001;
Weng et al., 2003
).
Transepithelial electrolyte secretion in Malpighian tubules of ants
(Formica polyctena) is also thought to be powered by the V-type
H+-ATPase located in the apical membrane of the tubule
(Weltens et al., 1992
).
Finding the V-type H+-ATPase in increasing numbers of Malpighian
tubules does not entirely rule out some role of the
Na+/K+-ATPase. The Na+/K+-ATPase
participates in transepithelial transport and cell volume regulation in
Malpighian tubules of Rhodnius prolixus
(Caruso et al., 2001
).
Serotonin, the primary diuretic agent in Rhodnius, inhibits the
Na+/K+ pump, thereby bringing about the stimulation of
transepithelial Na+ secretion
(Grieco and Lopes, 1997
). The
inhibition is thought to increase intracellular Na+ concentration,
which improves its competition for transport across the apical membrane. That
transepithelial secretion continues in the presence of ouabain confirms the
central role of the V-type H+-ATPase in powering transepithelial
transport (Beyenbach et al.,
2000
; Ianowski and O'Donnell,
2001
).
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Stimulating Na+ secretion |
---|
Electrophysiological studies of principal cells in Aedes
Malpighian tubules reveal the following effects of db-cAMP: a depolarization
of the basolateral membrane voltage together with a hyperpolarization of
similar magnitude of the transepithelial voltage
(Sawyer and Beyenbach, 1985).
In parallel with these voltage changes, the transepithelial resistance and the
fractional resistance of the basolateral membrane decrease, consistent with
cAMP increasing the Na+ conductance of the basolateral membrane
(Fig. 4). In addition, cAMP
activates a bumetanide-sensitive transport system, presumably
Na+/K+/2Cl- cotransport
(Hegarty et al., 1991
). In
summary, the initial Na+ diuresis observed in the blood-fed female
mosquito is mediated in part via the release of a CRF-like MNP into
the hemolymph. Binding to receptors in Malpighian tubules, MNP triggers the
synthesis of cAMP. In turn, cAMP activates Na+ channels and
Na+/K+/2Cl--cotransporters in the basolateral
membrane of principal cells. The entry of Na+ into the cell is
expected to increase cytoplasmic [Na+], thereby increasing its
competitive status for extrusion across the apical membrane and bringing about
the selective stimulation of transepithelial NaCl and water secretion. It
follows that the rate-limiting step of transepithelial Na+
secretion is entry across the basolateral membrane. By contrast, the
rate-limiting step for transepithelial K+ secretion is located at
the apical membrane.
|
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Stimulating K+ secretion |
---|
The high K+ conductance of the basolateral membrane further
explains why Malpighian tubules `prefer' to secrete K+ over
Na+ not only in the yellow fever mosquito but also in the weta
(Hemideina maori), ant (F. polyctena), blowfly (R.
prolixus), beetle (Onymacris rugatipennis) and cricket
(Teleogryllus oceanicus) (Neufeld
and Leader, 1998; Van
Kerkhove, 1994
; Weltens et
al., 1992
; Maddrell et al.,
1993
; Nicolson and Isaacson,
1990
; Marshall et al.,
1993
; Xu and Marshall,
1999a
). Malpighian tubules typically increase rates of
transepithelial fluid secretion with the increase in peritubular (hemolymph)
K+ concentration (Zhang et al.,
1994
). In the intact animal, an increase in hemolymph
[K+] is expected to immediately increase the cytoplasmic
[K+] in epithelial cells, thereby improving the competitive status
of K+ for extrusion across the apical membrane
(Fig. 3A). Thus, it appears
that the high K+ conductance of the basolateral membrane sets the
stage for the autoregulation of hemolymph K+ concentration, where
an increase in hemolymph K+ concentration prompts the immediate
increase in transepithelial K+ secretion. Autoregulation of
K+ excretion may be one reason why a K+-stimulated or
K+-dependent hormone to trigger a kaliuresis has not been
identified to date.
Next to K+ channels, carrier-mediated K+ entry
mechanisms across the basolateral membrane have been proposed in Malpighian
tubules of the cricket, fruit fly (Drosophila melanogaster), tobacco
hornworm (Manduca sexta) and blowfly
(Xu and Marshall, 1999b;
Rheault and O'Donnell, 2001
;
Reagan, 1995
;
Ianowski et al., 2002
). In
Malpighian tubules of ants, the K+ entry via K+
channels dominates when peritubular K+ concentration is high (113
mmol l-1), and entry via K+/Cl- and
Na+/K+/2Cl- cotransport takes over when the
peritubular K+ concentration is less than 51 mmol l-1
and 10 mmol l-1, respectively
(Leyssens et al., 1994
;
Van Kerkhove, 1994
). In
Malpighian tubules of A. aegypti, the stimulation of
Na+/K+/2Cl- cotransport by cAMP contributes
to the natriuresis that is observed (Fig.
4; Hegarty et al.,
1991
).
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Stimulating Cl- secretion |
---|
The analysis of fluid secreted by Aedes Malpighian tubules in the
presence of leucokinin-VIII revealed significant increases in the
transepithelial secretion of both NaCl and KCl, as if leucokinin made
Cl- more readily available for the transepithelial secretion with
Na+ and K+ (Table
3). Electrophysiological studies confirm this hypothesis:
leucokinin-VIII increased the transepithelial Cl- conductance
(Pannabecker et al., 1993). In
particular, the addition of leucokinin-VIII to the peritubular medium of
isolated Aedes Malpighian tubules leads to the immediate collapse of
the transepithelial voltage towards 0 mV together with a 6-fold decrease in
transepithelial resistance (Pannabecker et
al., 1993
). Low values of transepithelial voltage and resistance
are characteristic of so-called `leaky' epithelia, which are specialized to
transport solute and water at high rates. Thus, leucokinin-VIII turned a
moderately `tight' epithelium, with a transepithelial voltage of 59.3 mV
(lumen-positive) and a transepithelial resistance of 57.8
cm2, to a `leaky' epithelium, with a transepithelial voltage
of only 5.7 mV (lumen-positive) and a transepithelial resistance of only 9.9
cm2 (Pannabecker et al.,
1993
). The change took place with switch-like speed and was
equally quick to reverse upon washout of leucokinin
(Beyenbach, 2003
).
The diuretic effect of leucokinin is dependent on Cl-,
confirming the effect on a transport pathway taken by Cl-
(Hayes et al., 1989;
Pannabecker et al., 1993
). Two
Cl- transport pathways are possible. The laboratory of O'Donnell
has evidence for Cl- passing through stellate cells in
Drosophila Malpighian tubules
(O'Donnell et al., 1998
),
which was confirmed in the laboratory of Dow, where leucokinin increases
intracellular concentrations of Ca2+, the second messenger of
leucokinin, in stellate cells but not in principal cells
(Terhzaz et al., 1999
).
Although we found Cl- channels in the apical membrane of stellate
cells in Malpighian tubules of A. aegypti
(O'Connor and Beyenbach,
2001
), the preponderate evidence points to an extracellular
Cl- pathway activated by leucokinin. In particular, leucokinin
affects a single epithelial barrier such as that expected from the septate
(tight) junction located between the epithelial cells. The evidence for the
increase in the Cl- conductance of septate junctions in A.
aegypti Malpighian tubules is as follows: (1) transepithelial
Cl- diffusion potentials approach only 15% of Nernst potentials
under control conditions but 77% in the presence of leucokinin, signifying a
major increase in transepithelial Cl- conductance; (2) the large
symmetrical transepithelial Cl- diffusion potentials for both
lumen-to-bath and bath-to-lumen directed Cl- gradients are more
likely to be generated across a single barrier such as the septate junction
than across two cell membranes in series; (3) the effect of leucokinin on
transepithelial resistance is completely reversed by lowering the
Cl- concentration from 150 mmol l-1 to 5 mmol
l-1 in the extracellular, not intracellular, solutions
(significantly, the Cl- concentration must be lowered on both sides
of the epithelium to reverse the effects of leucokinin, testifying to an
extracellular Cl- pathway activated by leucokinin); and (4) the
observed electrophysiological changes from tight to leaky epithelium induced
by leucokinin can be explained only by an increase in paracellular
conductance. Finally, leucokinin also activates the transepithelial
Cl- conductance in tubules inhibited with cyanide or dinitrophenol,
pointing to a conductance change of a structure such as the septate junction
that is not immediately dependent on cell metabolism
(Beyenbach, 2003
;
Pannabecker et al., 1993
).
In the house cricket, leucokinin has diuretic effects similar to those in
Drosophila Malpighian tubules
(Coast, 2001;
Coast et al., 1990
).
Furthermore, Ca2+ mediates the effects of leucokinin in both
Acheta and Drosophila Malpighian tubules
(Coast, 1998
;
O'Donnell et al., 1998
). The
notable difference between the two species is that Malpighian tubules of the
cricket have no stellate cells (Coast,
2001
; Hazelton et al.,
1988
). Accordingly, the presence of stellate cells is not a
necessary condition for leucokinin to express its diuretic mechanism of
action. Indeed, recent studies in our laboratory have shown that stellate
cells are not needed to mediate the effects of leucokinin in Malpighian
tubules of A. aegypti (M. J. Yu and K. W. Beyenbach, submitted).
Wherever the signal transduction pathway of leucokinin has been studied,
Ca2+ has been found to serve as second messenger
(Coast, 1998). Actual
measurements of intracellular Ca2+ concentrations show that
leucokinin increases Ca2+ concentrations in stellate cells of
Malpighian tubules of the fruit fly
(O'Donnell et al., 1998
) and
in principal cells of the house cricket Malpighian tubules
(Coast, 1998
). Studies in our
laboratory have shown that extra- and intracellular Ca2+ are
necessary for signal transduction in Aedes Malpighian tubules
(Yu and Beyenbach, 2002
).
Particularly important is Ca2+ in the peritubular medium or
hemolymph. In the absence of peritubular Ca2+, leucokinin-VIII
produces only partial and transient (oscillating) attempts to produce the
leaky epithelial condition. To observe the full and lasting switch to the
leaky epithelium, Ca2+ must be able to enter the cell from the
peritubular medium or hemolymph. Nifedipine-sensitive Ca2+ channels
in the basolateral membrane of principal cells that are activated by
leucokinin mediate this Ca2+ entry. Detailed studies of the
relative roles of intra- and extracellular Ca2+ in Aedes
Malpighian tubules suggest the signal transduction sequence illustrated in
Fig. 5. Leucokinin binds to
G-protein-coupled receptor at the basolateral membrane of principal cells. The
leucokinin receptors that have been isolated from pond snails (Lymnaea
stagnalis), cattle ticks (Boophilus microplus) and the fruit fly
have a sequence consistent with a G-protein coupled receptor
(Radford et al., 2002
;
Holmes et al., 2003
).
Furthermore, AlF4-, a known activator of G-proteins,
duplicates the effects of leucokinin in Aedes Malpighian tubules
(Yu and Beyenbach, 2001
).
Stimulation of the G-protein is thought to activate phospholipase C and to
generate inositol (1,4,5)-trisphosphate and diacylglycerol. IP3
goes on to release intracellular Ca2+ from stores. The subsequent
rise in cytoplasmic Ca2+ concentration and/or the depletion of
intracellular Ca2+ stores activates Ca2+ channels in the
basolateral membrane. Extracellular Ca2+ entering the cell produces
and maintains the epithelium in the leaky condition as long as leucokinin is
present. How Ca2+ or other agents bring about the increase in
junctional conductance or permeability is currently an active field of
investigation (Beyenbach,
2003
). Stellate cells may well mediate transepithelial
Cl- secretion under control conditions in Aedes Malpighian
tubules. However, in the presence of leucokinin, a septate junctional
Cl- conductance mediates transepithelial Cl- secretion
in the presence of leucokinin.
|
In view of the non-selective stimulation of NaCl, KCl and water secretion, leucokinin may be a regulator of hemolymph volume in insects. In freshwater larvae, leucokinin may participate in the excretion of osmotic water loads by delivering large quantities of isosmotic fluid to distal Malpighian tubules, hindgut and rectum for urinary dilution. Leucokinin may also be useful in the eclosion diuresis, reducing the flight payload as the adult insect takes its first flight after leaving pupal aquatic habits behind. Furthermore, leucokinin might potentiate the diuresis on gorging occasions, synergistically integrating with other intrinsic and extrinsic mechanisms of diuresis.
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Concluding thoughts |
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Acknowledgments |
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