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First published online January 19, 2006
Journal of Experimental Biology 209, 475-483 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02035
Heterogeneous perfusion of the paired gills of the abalone Haliotis iris Martyn 1784: an unusual mechanism for respiratory control
School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch 8020, New Zealand
* Author for correspondence (e-mail: Norman_Ragg{at}yahoo.co.uk)
Accepted 13 December 2005
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: abalone, bipectinate gill, haemolymph, oxygen uptake, branchial perfusion, cardiac output
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
Amongst gastropods, the need to accommodate the visceral organs within a
coiled shell has led to a characteristic reduction or loss of the ancestral
right-side organs (e.g. Voltzow,
1994). However, a small number of extant gastropod families,
including the Haliotidae or abalone, have retained functional right-side
organs. Haliotids are not perfectly bilaterally symmetrical; the visceral
organs are displaced to the left by the large right shell adductor muscle
(Yonge, 1947) and, although
both right and left kidneys are present, they are morphologically and
functionally disparate (Harrison,
1962) and have lost specific association with the right or left
side vasculature (Crofts, 1929;
Bourne and Redmond, 1977;
Russell and Evans, 1989).
However, the bipectinate right and left gills (ctenidia) are morphologically
similar (Crofts, 1929), are
supplied from a common haemolymph sinus and deliver haemolymph into the left
and right auricles of the heart, respectively. Thus, the gills and associated
vasculature are believed to closely resemble the ancestral condition.
Recent investigations of gas exchange in Haliotis iris have
demonstrated that the gills are responsible for essentially all oxygen uptake
under both normoxia and hypoxia and are capable of high oxygen extraction
efficiencies (Taylor and Ragg,
2005). The authors have also shown that ventilation, perfusion and
diffusion are well matched in the right gill of H. iris (Ragg and
Taylor, in press). The current study extends these observations by considering
the overall efficiency of the two gills and, in particular, the capacity of
the gill system to accommodate increased oxygen demand by adjustments to
branchial haemolymph flow following a period of internal hypoxic stress.
Changes in left and right post-branchial oxygen pressures were measured by
sampling from chronic indwelling cannulae, and haemolymph flows in the left
and right efferent ctenidial veins were recorded by means of pulsed Doppler
flow probes. It is demonstrated that the circulatory responses of the left and
right gills are, in fact, quite different.
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Materials and methods |
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Experimental design
Measurements were made on animals in three states, defined as follows.
). ). Sets of measurements of oxygen partial pressure in haemolymph samples from the left and right efferent ctenidial veins (PaO2), and in the exhalant water, were obtained in triplicate for each animal in each of the above states. Continuous records of haemolymph flow in each vessel and heart rate were obtained throughout the period of haemolymph sampling (2-3 min per sample). On several occasions, animals exhibited avoidance behaviour, either clamping to the chamber floor or raising and twisting the shell. Measurements were also made under these activity conditions.
Animal preparation
Abalone were starved for 24 h prior to manipulations, which took place in
moist air at 4-6°C. A high-speed diamond grinding wheel (DremelTM;
Emerson Electric Co., St Louis, MO, USA) was used to cut two openings in the
shell. One opening (20x10 mm) exposed the right efferent ctenidial vein
posterior to the shell apertures. A second (40x10 mm), cut ventrally to
the first, exposed the left mantle surface. Two 1.5 mm holes were drilled
through the shell either side of the pericardial region, and impedance leads
(0.2 mm insulated copper wire, coiled bared ends contacting the mantle
epidermis) for recording of cardiac activity were inserted and secured with
cyanoacrylate glue. The animals were given a minimum of 2 days to recover in
the holding system.
Once recovered, i.e. alert and feeding and showing no sign of tissue damage or haemorrhage, each abalone was cannulated, and customised Doppler probes were inserted to measure blood velocity. A 1 mm2 crystal sub-assembly (Iowa Doppler Products, Iowa City, IA, USA) was encased in epoxy resin and attached to a 5 mm section of 0.86 mm (i.d.) polyethylene tubing. PVC wings were attached to the tubing to prevent rotation once in position against the vessel wall. The cannula, a 20 cm length of 0.6 mm (i.d.) x 0.8 mm (o.d.) PE tubing with a tapered end was threaded through the sleeve of the pulsed-Doppler assembly. A 23-gauge needle was used to puncture the right efferent ctenidial vein approximately 10 mm anterior to the pericardium, and 5 mm of cannula was inserted retrograde to haemolymph flow. The cannula was tested for patency and secured to the shell with cyanoacrylate glue. The Doppler crystal assembly was then manoeuvred onto the mantle surface immediately posterior to the cannula insertion point, and its leads secured to the shell by means of a friction mount, permitting subsequent minor adjustments in crystal position. The left efferent ctenidial vein, located by displacing the mantle roll dorsally, was prepared in a similar way, using a U-shaped cannula.
The cannulae were stoppered, the impedance and Doppler leads connected and the animal placed into an experimental chamber. Each chamber consisted of a 1.0-litre circular polycarbonate bowl supplied with 15°C seawater from a recirculating reservoir. The cardiac leads were connected to an impedance coupler (A100; Strathkelvin Instruments, Glasgow Strathclyde, UK), and Doppler signals were processed using a directional pulsed-Doppler flowmeter (20 MHz; 545C-4; Bioengineering, Iowa City, IA, USA). Output was digitally recorded using PowerLabTM 4/20 (ADInstruments, Bella Vista, NSW, Australia) data acquisition hardware and ChartTM 4.1.2 (ADInstruments) software.
Haemolymph flow measurement
Signals from the left and right efferent ctenidial probes were acquired
simultaneously. Minor adjustments were made to the crystal positions and range
settings until a maximal signal was obtained. The mean Doppler output was
calculated by integration over the whole sampling period (
5 min).
Calibration of the Doppler signal in terms of volumetric flow was achieved by two methods. In situ calibration was attempted for each crystal placement. At the end of the experiment the abalone was decapitated and the ventricle cut to create a low-resistance outflow path. A suspension of zeolite particles (<80 µm, filtered barbecue deodorizer) in seawater was passed through each cannula at a range of preset flows via a peristaltic pump, and the mean Doppler signals were recorded and used to create the calibration curve.
In the second calibration technique, geometric assumptions were used to
calculate the flow velocity using the `Doppler equation'
(University of Iowa Bioengineering,
1986; Levick,
1991):
 | (1) |
where V is the mean velocity of blood across the vessel diameter
(mm s-1), Fd is the Doppler shift frequency (in
this case 0.5 V
1 kHz shift), C is the velocity of sound in
blood (1 565 000 mm s-1), Fo is the transmitter
frequency (20 000 kHz) and A is the angle between the beam and the
blood velocity vector (assumed to be 45°).
Vessel cross-sectional area was determined by low-pressure injection of amaranth-stained gelatin dissolved in seawater (1:15 w/w). Transverse sections of the fixed tissues (70% ethanol) were photographed, and internal cross-sectional area (Fig. 1A) was measured using image analysis software (Scion ImageTM beta 4.0.2; www.scioncorp.com). The product of vessel cross section and mean velocity thus gave an estimate of mean flow.
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The Doppler equation assumes that the vessel is circular in section and
that blood flow is laminar with a parabolic profile. In such cases, the
maximum midstream flow is twice the mean flow velocity
(University of Iowa Bioengineering,
1986; Vogel,
1994). The efferent ctenidial veins of abalone clearly are not
perfectly circular due to the presence of a thick band of connective and
`lymphoid' tissue transecting the lumen
(Fig. 1A;
Crofts, 1929). The assumption
of parabolic flow was therefore tested by plotting the Doppler signal strength
against focal depth, which was increased in 50 mV (0.5 mm penetration)
increments.
Geometric flow estimates were more variable and lower (74.5±11.7%, N=13) than those determined by known-flow calibration. Geometrically calibrated flows were accordingly corrected using this factor to provide the best estimate of flow and only used when known-flow calibration was unavailable.
Oxygen partial pressure and content
A syringe (Hamilton GastightTM; 25-gauge) was used to withdraw 100
µl of haemolymph from the cannula line to clear dead-space and `prime' the
oxygen electrode (MI730; Microelectrodes Inc., Bedford, NH, USA; Cameron water
jacket at 15°C; Cameron Instruments, Guelph, ON, Canada; 781b oxygen
meter; Strathkelvin Instruments). A further 100 µl were then withdrawn and
injected into the electrode chamber, and PO2
was recorded after a 2 min stabilizing period. As left and right efferent
ctenidial samples could not be taken simultaneously, they were taken in random
order, within 5 min of each other. Seawater PO2
was also measured in conjunction with each set of haemolymph samples.
Circulating water in the experimental container was taken to represent
inhalant PO2. Branchial chamber water was
sampled via a PVC cannula briefly inserted 2 mm through the
second oldest patent shell hole; this was assumed to represent exhalant water
(after Volzow, 1983).
Oxygen contents (CO2; mmol l-1)
of haemolymph samples were calculated from PO2
values (mmHg; 1 mmHg133 Pa) using oxygen binding curves determined for
the same population of H. iris. As haemolymph
PO2 values observed here (80-105 mmHg) lay well
above the P50 for H. iris haemocyanin (4-12 mmHg;
Behrens et al., 2002), a linear
relationship provided a satisfactory fit (slope 0.00199±0.00033 mmol
l-1 mmHg-1; intercept 0.178±0.022 mmol
l-1; N=139). Oxygen convection in the efferent ctenidial
flow was therefore calculated as the product of
CO2 and flow rate.
Data are expressed as means ± standard error of the mean (s.e.m.). Statistical analyses were carried out using StatisticaTM 6.0 software (StatSoft, Inc., Tulsa, OK, USA), using model I analysis of variance (ANOVA) with replicate samples nested within individual animal, followed by Fisher's least significant difference pairwise comparison of means. Statistical significance was accepted at P<0.05.
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Results |
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Doppler calibration
A transverse flow profile was constructed for the right efferent ctenidial
vein of 12 individuals. In all cases, a reasonable approximation of parabolic
flow was observed (Fig.
1B).
Haemolymph flow
In stressed animals immediately following handling, total haemolymph flow
through both gills was 24.4±3.6 ml kg-1 min-1
(N=13). This increased non-significantly to 25.8±5.7 ml
kg-1 min-1 (N=8) in recovering animals and
declined highly significantly to 9.1±2.1 ml kg-1
min-1 at rest (N=5, P<0.001).
There were marked differences in the relative perfusion of the left and right gills dependent upon animal state (Fig. 2). In stressed animals, mean right gill haemolymph flow was 10.77±1.37 ml kg-1 min-1 (N=14). During the recovery period, mean right gill flow was 5.86±1.59 ml kg-1 min-1 (N=9) and in settled animals it was 8.56±1.95 ml kg-1 min-1 (N=6). These values were not significantly different. By contrast, mean left gill flow was 13.32±2.63 ml kg-1 min-1 (N=14) in stressed animals, this was elevated (non-significantly) to 18.20±5.75 ml kg-1 min-1 (N=9) during recovery but decreased highly significantly by a factor of more than 30 to 0.41±0.34 ml kg-1 min-1 (N=6) in settled animals (P<0.001). That is, at rest, more than 95% of the respiratory haemolymph flow was carried by the right gill.
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Haemolymph PO2 values were used to calculate oxygen contents from oxygen binding data (see Materials and methods) and were combined with efferent ctenidial flow rates to estimate the total output of oxygen from the gills (Fig. 4). In stressed abalone, the total post-branchial oxygen convection was 0.0075±0.0015 µmol g-1 min-1 falling significantly to 0.0027±0.0006 µmol g-1 min-1 in settled animals. Despite the higher post-branchial haemolymph PO2 recorded in the left gill of settled animals, its contribution to total oxygen uptake was minimal because of the very low haemolymph flow.
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Heart rate
No significant change in heart rate was associated with the greatly
decreased gill perfusion in resting animals compared with stressed animals
(28.5±0.9 min-1 and 28.2±1.1 min-1,
respectively). A small but significant increase in heart rate was observed
during the recovery period (31.8±0.8 min-1;
P=0.009).
The effects of activity
In 12 individuals, spontaneous activity was displayed during a period of
data recording. Responses varied but some general patterns were apparent. At
the onset of clamping (Fig. 5)
or twisting (Fig. 6), the
heartbeat became erratic or was arrested. During twisting
(Fig. 6), the impedance signal
was disrupted by the large body movements, but efferent ctenidial flow clearly
fell to zero in the left gill and became intermittent in the right gill. A
normal impedance signal was rapidly re-acquired after cessation of twisting
(<20 s). Resumption of the regular heartbeat was followed by flow through
the right and then the left gill, typically after an interval of 5-15 cardiac
cycles. In animals that clamped for more than 60 s, this recovery pattern
ensued regardless of whether the animal released its clamp or not
(Fig. 5).
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; Baldwin et al.,
1992; Wells and Baldwin,
1995; Behrens et al.,
2002).
The increased branchial blood flow would tend to promote increased oxygen
uptake from the seawater and may be interpreted as one component of a suite of
responses that contribute to the metabolic scope of abalone. Oxygen
consumption was not measured in the present experiments so it remains unclear
whether this was actually enhanced in the recovering animals. As discussed
elsewhere (Taylor and Ragg,
2005), external water currents are required to augment the
endogenous ciliary ventilation for maximum aerobic scope in H. iris.
Nevertheless, increases in oxygen uptake by factors of 2.5-3.5 have been
observed in crawling H. kamschatkana (Donovan and Carefoot,
1997,
1998) and by a factor of 1.9 by
H. laevigata in response to elevated environmental ammonia
(Harris et al., 1998).
In the absence of external water currents, the mean rate of oxygen uptake
from seawater was previously reported as 0.47 µmol g-1
h-1 for intact settled H. iris
(Taylor and Ragg, 2005) and
slightly higher in recently cannulated abalone (0.54 µmol g-1
h-1; Ragg and Taylor, in press). Based on the flow rates and
estimated oxygen contents of haemolymph in the efferent ctenidial veins, the
total convection of oxygen (bound and dissolved) in the post-branchial
haemolymph was only 0.16 µmol g-1 h-1 in settled
abalone and 0.45 µmol g-1 h-1 in stressed animals
(Fig. 4). Care was taken to
standardize conditions with those of previous respirometry trials: the
possibility remains, however, that animals in the current experiment displayed
unusually low oxygen uptake rate
(
O2). The
authors suggest, however, that given that a substantial venous reserve is
usually present (Ragg and Taylor, in press), these data imply that a
significant proportion of oxygen uptake may not enter the post-branchial
haemolymph. As virtually the whole of oxygen uptake is known to be abstracted
from the branchial water flow (Taylor and
Ragg, 2005), the possibility of direct uptake by metabolically
active integumental surfaces within the branchial chamber (e.g. ciliary
epithelia, mucous glands), or adjacent organs, requires further
investigation.
Apart from a minor vascular route through the right mantle, the whole of
the systemic venous return to the heart passes through the left and right
gills (Crofts, 1929;
Ragg, 2003;
Taylor and Ragg, 2005). Thus,
total gill flow, which increased 2.7 times from 9.1 ml kg-1
min-1 at rest to 24.4 ml kg-1 min-1 in
stressed abalone, would have corresponded closely to cardiac output under
these conditions. However, cardiac frequency was constant at about 28
min-1 confirming previous observations
(Taylor and Ragg, 2005) of its
insensitivity to disturbance and activity status. It is therefore deduced that
cardiac compensation in H. iris resulted solely from adjustments to
stroke volume, i.e. increasing from 0.37±0.15 ml kg-1 live
mass at rest to 0.99±0.21 ml kg-1 in disturbed abalone.
Heart rates recorded for H. iris are slightly higher than those of
the similar sized abalone H. rubra (25 min-1;
Russell and Evans, 1989) and
H. corrugata (21 min-1;
Bourne and Redmond, 1977).
Heart rate more closely resembles that of the smaller H. discus
hannai (32 min-1 at 15°C;
Fujino et al., 1984). The
smaller (50 g) and relatively active gastropod Hemifusus tuba
showed a slower heart rate than H. iris (18 min-1 at
15°C; Depledge and Phillips,
1986) but a larger stroke volume, resulting in a cardiac output of
approximately 50 ml kg-1 min-1. Resting decapod
crustaceans of a corresponding size to H. iris typically exhibit
rather higher rates of 30-50 min-1; however, as with H.
iris, increased stress or activity have minimal effect on heart rate
(McMahon and Wilkens,
1983).
Heterogeneity in right and left gill perfusion
An important conclusion from the present study is that adjustments to
cardiac output and respiratory blood flow were accommodated almost entirely by
changes in the perfusion of the left gill - from more than 75% of total flow
in recovering abalone to less than 5% at rest. Heterogeneous perfusion, and
circulatory switches between different gas exchangers, occur in animals in
which there are clear differences in exchanger morphology, e.g. in relation to
bimodal respiration in crustaceans (Taylor
and Greenaway, 1984; Taylor
and Taylor, 1992) and vertebrates
(Johansen, 1982) but this
appears to be the first report with respect to paired organs.
These changes in respiratory blood flow probably were not accompanied by
corresponding changes in ventilation, as endogenous ciliary ventilation was
similar in recently handled abalone and after settling overnight
(Taylor and Ragg, 2005). In
fishes, regulation of gas exchange does not involve shutdown of whole gills,
but at rest the number of perfused lamellae may be reduced by as much as 60%
(Jones and Randall, 1978;
Randall and Daxboeck, 1984;
Farrell and Jones, 1992). As
in abalone, the under-perfused lamellae are still ventilated. Similarly,
amphibians reliant upon cutaneous gas exchange may recruit additional surface
capillaries during increased O2 demand, in the absence of obvious
augmentation to ventilation (Feder,
1995).
In decapod crustaceans, a superficially analogous shutdown of gas exchange
in one branchial chamber occurs during bouts of unilateral scaphognathite
ventilation, although no left or right bias has been noted
(Mangum, 1983;
McMahon and Wilkens, 1983). In
decapods, preferential perfusion of the ventilated gills may be effected by
the associated changes in branchial transmural pressures
(Taylor, 1990) but it is
unlikely that flow ceases on the non-ventilated side. Non-perfusion of a
gas-exchanger module is probably not a viable strategy for crustaceans and
other higher taxa because of the attendant risk of thrombosis. By contrast,
gastropod haemolymph lacks clotting factors
(Armstrong et al., 1971;
Taylor et al., 1994).
The gills of H. iris are supplied from a common venous
compartment, the basibranchial sinus
(Crofts, 1929;
Ragg, 2003). As the constant
volume model for the operation of the molluscan heart
(Ramsay, 1952;
Fretter and Graham, 1994)
precludes any obvious mechanism for differential aspiration by the left and
right auricles, large changes in the relative flow through the left and right
gills must be associated with changes in the relative resistance of the
perfusion paths. The contractility and vasoactivity of molluscan vessels in
response to neuropeptides and bioamines is well established (e.g.
Aplysia, Brownell and Ligman,
1992; H. kamtschatkana, Krajniak and Bourne,
1987,
1989). Varicose nerve fibres
showing 5-hydroxytryptamine immunoreactivity are present in the walls of blood
vessels of H. rubra, including the afferent ctenidial veins
(Russell and Evans, 1989).
However, a marked pulsatility observed in the reduced left gill flow suggests
that resistance changes occurred in the gill itself rather than downstream in
the efferent ctenidial veins. The vessels associated with the gills of H.
iris are certainly muscular and are capable of lumen adjustment
(N.L.C.R., unpublished observation). Longitudinal muscle blocks associated
with cartilage on either side of the efferent ctenidial veins could obliquely
distort the ctenidia and affect efferent drainage and therefore are also
potential sites of flow control (Ragg,
2003). Clearly, the relative responsiveness of abalone ctenidia to
vasoactive agents deserves further investigation.
In the constant volume model (Ramsay,
1952; Fretter and Graham,
1994), ventricular systole causes passive expansion of the two
approximately equal-sized auricles by transmission of negative pressure
through the pericardial fluid. Thus, reduced flow in the left efferent
ctenidial veins could potentially deprive the left auricle of haemolymph.
However, this is probably not the case. The left auricle is connected to the
right efferent ctenidial vein by a valved vascular route passing through the
left kidney (Crofts, 1929;
Ragg, 2003). It therefore
appears that when the left branchial resistance is increased, haemolymph is
partially diverted from the right efferent ctenidial vein to the left auricle.
In support of this suggestion is the observation that casting resin perfused
at low pressure into the right efferent ctenidial vein preferentially passes
through the left kidney and fills the left auricle before the right.
Gill perfusion during activity
Bourne and Redmond (1977)
noted that the onset of activity in H. corrugata caused a transient
hydrostatic pressure spike throughout the vascular system. As no pressure
gradient was developed, they predicted that haemolymph flow would not be
assisted by these muscular contractions. Direct flow recordings taken from the
gills of H. iris during twisting and clamping corroborate this
suggestion, and in fact branchial haemolymph flow was reduced due to cardiac
arrest (Figs 5,
6). Aortic pressure traces from
H. midae also show evidence of cardiac arrest with the onset of
clamping (Trueman and Brown,
1985). Cardiac arrest may help prevent damage to the heart by
pressure surges, as proposed for the tarantula Eurypelma californicum
during hydraulic leg extension (Paul,
1986). Interestingly, when avoidance activity was sustained in
H. iris, normal heart rate resumed, followed by renewed flow through
the right gill. However, the left gill typically remained unperfused until
activity ceased (Figs 5,
6).
Diffusion limitation in right and left gills
In an earlier study (Ragg and Taylor, in press), the performance of the
right gill was analyzed in terms of oxygen extraction, ventilation perfusion
ratio, diffusive conductance and the diffusion limitation index,
Ldiff (Piiper,
1982). Based on these criteria, it was concluded that the right
gill operated efficiently and near optimally. Right gill
Ldiff values of 0.5 were obtained for settled
abalone, indicating that neither perfusion nor the diffusive conductance of
the gill prevailed to limit the rate of oxygen transfer. Prebranchial oxygen
partial pressure measurements were not obtained in the present study but,
using the earlier values for resting animals (37.3±3.6 mmHg) and values
obtained from a separate subset of abalone subjected to emersion and exercise
(32.2±3.8 mmHg, N=12; N.L.C.R., unpublished observations), the
Ldiff of the right gill was estimated to be
0.40±0.6 and 0.44±0.8 for resting and stressed animals,
respectively. By contrast, the left gill was highly perfusion limited at rest,
with an estimated Ldiff of 0.14±0.07. This rose to
0.46±0.07 in stressed animals. Adjustments to perfusion of the left
gill therefore play an important role in the control of oxygen delivery in
this animal.
Conclusions
An unusual gas exchange strategy has been revealed in the abalone
Haliotis iris. The right gill appears to be perfused at a fairly
constant rate, regardless of demand. The left gill, however, is chronically
under-perfused in resting H. iris, to the extent that haemolymph flow
almost ceases. Thus, oxygen taken up by the right gill, plus direct oxygen
diffusion into peripheral tissues, effectively supports the routine metabolism
of the abalone. During periods of increased oxygen demand, perfusion rates in
the left gill increase approximately 30-fold, matching oxygen uptake of the
right gill. Changes in oxygen uptake at the left gill therefore effectively
support the metabolic scope of the abalone. The mechanisms determining
differential gill resistance warrant further investigation, in particular the
role of neurohormones. The greater flexibility in blood flow exhibited by the
left gill is of interest in relation to the evolutionary abandonment of the
paired gill design, i.e. the loss of the right gill by higher gastropods.
Comparative studies examining the strategies utilised by pectinibranch snails
to regulate oxygen uptake would therefore be of considerable interest.
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Acknowledgments |
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