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First published online March 16, 2007
Journal of Experimental Biology 210, 1216-1224 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.002881
Maximum cardiac performance and adrenergic sensitivity of the sea bass Dicentrarchus labrax at high temperatures
1 UBC Centre for Aquaculture and the Environment, Faculty of Agricultural
Sciences and Department of Zoology, 2357 Main Mall, University of British
Columbia, Vancouver, BC, V6T 1Z4, Canada
2 Göteborg University, Department of Zoology, PO Box 463, SE-405 30,
Göteborg, Sweden
3 University of Linköping, Department of Biology, IFM, SE-581 83,
Linköping, Sweden
4 Institut des Sciences de l'Evolution, Département de Biologie
Intégrative, 1 Quai de la Daurade, 34200 Sète, France
* Author for correspondence (e-mail: farrellt{at}interchange.ubc.ca)
Accepted 6 February 2007
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Summary |
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Key words: sea bass, heart, cardiac output, heart rate, temperature, adrenaline
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). As such, temperature optima exist for maximum oxygen
uptake, aerobic scope and maximum prolonged swimming speed (i.e. critical
swimming speed, Ucrit), but these may vary among fish
species and perhaps even among different stocks within a species
(Brett, 1971;
Beamish, 1978;
Randall and Brauner, 1991;
Johnston and Ball, 1997;
Taylor et al., 1996;
Lee et al., 2003a;
Claireaux et al., 2005). Given
that temperature influences fish distributions and their migrations, there is
great interest in understanding why swimming performance declines at high
temperature, particularly in an era of global climate change and warming of
rivers, lakes and seas.
The discovery of parallel declines in maximum oxygen uptake, aerobic scope
and Ucrit for salmon led to the suggestion of a
cause–effect relationship between declining oxygen delivery and swimming
performance (Brett, 1971).
Mechanistically, Brett suggested that this relationship results from a failure
of gill ventilation to deliver sufficient water to compensate for the decrease
in water oxygen content as temperature increases
(Brett, 1971). Accordingly,
decreases in oxygen content of arterial and venous blood occur with increasing
water temperature in resting rainbow trout Oncorhynchus mykiss
(Heath and Hughes, 1971). In
addition, this study revealed cardiac arrhythmias as venous oxygen content
fell towards zero, an observation that leads to the alternative suggestion
that the decrease in oxygen tension in venous blood limits oxygen supply to
the cardiac muscle and that this cardiac oxygen deficiency contributes to the
decrease in performance of salmonids at high temperature
(Farrell, 1997). Others have
suggested that the problem may lie with oxygen delivery to tissues
(Taylor et al., 1996;
Pörtner, 2002;
Farrell, in press).
While it remains difficult to separate out the proximate cause(s) for the
failure of performance, temperature optima for maximum cardiac performance
have been clearly defined for salmonids
(Brett, 1971;
Farrell et al., 1996;
Taylor et al., 1996;
Mercier et al., 2002).
However, we know little of the temperature sensitivity of maximum cardiac
performance in non-salmonids. Recently, temperature optima were shown for
routine cardiac performance and oxygen uptake in Atlantic cod Gadus
morhua, with cardiac output collapsing near the critical thermal maximum
(Gollock et al., 2006). These
recent findings extend considerably on earlier work with Atlantic cod
(Lannig et al., 2004) that
provided evidence for a constraint on blood flow at high temperature.
Arrhythmia is commonly considered an early signal of cardiac failure in
both mammals and fish (e.g. Heath and
Hughes, 1971; Chatelier et al.,
2005a), but the problem may be more complex than a deficient
myocardial oxygen supply. Calcium handling during excitation–contraction
coupling and a collapse of adrenergic stimulation, as well as extracellular
acidosis and hyperkalemia, have also been implicated
(Farrell, 1997;
Hanson et al., 2006;
Farrell, in press). With
higher heart rates, there is a shorter active state at high temperature
(Vornanen, 1998), and so a
more rapid flux of calcium through the sarcolemmal L-type calcium channel is
needed to maintain tension development. The main modulator of the open state
of this channel is ß-adrenergic stimulation, as shown in both fish
(Vornanen, 1998;
Shiels and Farrell, 2000) and
mammals (Reuter, 1983).
However, it has been shown in rainbow trout that this modulator becomes
increasingly less effective as acclimation temperature increases, with the
result that adrenergic stimulation of cardiac inotropy decreases at high
temperature (Ask et al., 1980;
Keen et al., 1993;
Shiels and Farrell, 2000;
Shiels et al., 2002;
Shiels et al., 2003). In fact,
the perfused rainbow trout heart becomes almost refractory to adrenaline at a
temperature above 18°C, which appears to be the optimum temperature for
maximum performance in this species
(Farrell et al., 1996).
Adrenergic stimulation is also critical in protecting the fish heart from the
debilitating extracellular hypoxia, acidosis and hyperkalemia
(Gesser and Jorgensen, 1982;
Gesser et al., 1982;
Farrell et al., 1984;
Farrell, 1985;
Driedzic and Gesser, 1994;
Nielsen and Gesser, 2001;
Andersen et al., 2004)
associated with maximal performance such that the rainbow trout heart can
perform maximally at a lower oxygen tension with maximum adrenergic
stimulation than without it (Hanson et
al., 2006). This protective adrenergic effect diminishes at high
temperature (Hanson and Farrell, in
press), and is further compounded by rainbow trout swimming with a
greater anaerobic locomotory effort at high temperature
(Jain and Farrell, 2003;
Lee et al., 2003b) that then
heightens the extent of the extracellular acidosis and hyperkalemia. We were
interested in discovering whether non-salmonids also show limited adrenergic
inotropy at high temperature, knowledge that would be important in our general
understanding of why maximum cardiac performance in fish is limited at high
temperature. Consequently, the present study assessed maximum cardiac capacity
and adrenergic stimulation at high temperatures in the European sea bass
Dicentrarchus labrax. Sea bass lack a coronary circulation, and so we
could be certain that changes in venous blood composition directly influence
the entire myocardium, unlike in salmonids where the presence of a coronary
circulation confounds matters.
Sea bass are a representative of the Moronidae, which are found in
fresh and brackish water, as well as in coastal marine areas of eastern North
America, Europe and northern Africa. Sea bass are found throughout the
Mediterranean Sea and along the eastern coast of Europe from Portugal to
Norway. They are active predators (feeding on fish and crustaceans) and live
in small shoals as juveniles. As adults (up to 100 cm; 12 kg), sea bass are
powerful swimmers that inhabit dynamic depths ranging from 1 to 100 m.
Temperature but not salinity (Chatelier et
al., 2005b) has a strong influence on their performance. For
instance, between 10°C and 20°C, standard and active metabolic rates
increase 2.5- and 5.5-fold, respectively
(Claireaux and Lagardere,
1999). Optimal temperatures for metabolic scope and
Ucrit are 22°C and 27°C, respectively
(Claireaux et al., 2006;
Claireaux and Lagardere,
1999). Temperatures below 9–10°C are too cold for
reproduction and, in the English Channel, adult sea bass over-winter offshore,
while non-maturing juveniles remain inshore
(Pickett and Pawson, 1994).
Similar to salmonids, sea bass are athletic swimmers but their cardiac anatomy
is markedly different. The sea bass ventricle does not receive any oxygenated
blood via a coronary circulation while salmonids have a
well-developed arterial supply of oxygen to the compact myocardium
(Axelsson and Farrell, 1993;
Gamperl et al., 1995). The aim
of the present study was to investigate whether maximum cardiac performance
and the effect of adrenergic stimulation differ in sea bass compared to
salmonids.
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Materials and methods |
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; oxygen: >85%
air-saturation). Fish were exposed to natural photoperiod and were fed a
commercial diet (Bar D Perform Natura 4.5, SICA du Gouessant, BP 228, Lamballe
22402, France). Cardiac assessments were made at these two acclimation
temperatures to examine phenotypic plasticity.
In situ perfused heart studies
Cardiac performance studies were conducted on six fish at both 18°C
(body mass=252±4 g; ventricular mass=0.252± 0.009 g; relative
ventricular mass=0.100±0.003%) and 22°C (body mass=318±6 g;
ventricular mass=0.248±0.005 g; relative ventricular
mass=0.078±0.001%). Maximum cardiac performance was assessed with the
Farrell in situ fish heart preparation (see
Farrell et al., 1986), with
the modifications outlined by Farrell et al.
(Farrell et al., 1988) and
Mercier et al. (Mercier et al.,
2002). Fish were first anaesthetised by 0.05 g
l–1 tricaine methane sulphonate (MS222), buffered with 0.05 g
l–1 NaHCO3, and placed in an operating sling where
the gills were irrigated with a lower concentration of anaesthetic (0.02 g
l–1 MS222 buffered with 0.02 g l–1
NaHCO3). The heart was isolated in terms of saline input and output
by securing stainless steel input and output cannulae into the sinus venosus
via a hepatic vein and the ventral aorta, respectively, while leaving
the heart undisturbed and pericardium intact. Cardiac perfusion was started
immediately using oxygenated saline containing a tonic level of adrenaline (5
nmol l–1 AD; adrenaline bitartrate, Sigma-Aldrich, St
Quentin-Fallavier, France). The preparation was then immersed in a
saline-filled, temperature-controlled organ bath at the appropriate
acclimation temperature (18°C or 22°C), with the input and output
cannulae attached to constant pressure heads. A 15–20 min period of
control perfusion preceded any assessment, during which the filling (input)
pressure of the heart was set to give a routine cardiac output
(
=ventral aortic flow in the output
cannula) of 25 ml min–1 kg–1 body mass and
mean output pressure was set at 
5 kPa to simulate routine in
vivo ventral aortic blood pressures. Maximum
was established with stepwise
increases in filling pressure (i.e. a Starling response) until
reached a plateau. Diastolic output
pressure was then increased with the heart pumping maximally until a maximum
cardiac power output was reached. The heart was then returned to the control
perfusion conditions for a 15 min recovery and an equilibration with a new
perfusate adrenaline concentration (10 nmol l–1, 50 nmol
l–1, 100 nmol l–1 and 500 nmol
l–1). The adrenaline concentration range spanned that
observed in plasma of resting and stressed rainbow trout (e.g.
Milligan et al., 1989;
Gamperl et al., 1994) and
therefore resulted in a tonic through to a maximal adrenergic stimulation of
the sea bass heart. With the perfused sea bass heart, great care was needed to
prevent excessive increases in output pressure. Occasionally at 18°C and
more frequently at 22°C, an excessive output pressure produced
irreversible cardiac failure that was not alleviated by either restoring
control conditions or increasing the adrenaline concentration. These partial
data sets were not used for the general data analysis presented here, although
the heart had performed well up to this point. An in-line Transonic flow probe
(Transonic Systems, Ithaca, NY, USA) was used to record
. Pressures in the sinus venosus
(input) and ventral aorta (output) were measured with pressure transducers
(model DPT-6100, pvb Medizintechnik, Germany), through saline-filled tubes
placed at the tip of the cannulae. The pressure transducers were calibrated
against a static water column with each preparation. Pressure and flow signals
were amplified (4ChAmp amplifier, Somedic, Sweden) and stored with a
custom-made data acquisition program, General Acquisition (Labview version
6.01, National Instruments, USA). The perfusate (pH 7.8 at 15°C) contained
(in mmol l–1): NaCl, 124; KCl, 3.1;
MgSO4.7H2O, 0.93; CaCl2.2H2O,
2.52; glucose, 5.6 TES (N-tris[hydroxymethyl]methyl-2-aminoethanesulphonic
acid) salt, 6.4; and TES acid, 3.6 (Keen
and Farrell, 1994). The TES buffer system simulated the buffering
capacity and temperature dependency
(dpKa/dT=0.016 pH units
°C–1) of rainbow trout plasma. By equilibrating the
saline with 100% O2, the oxygen gradient between the saline and the
myocardium was at least 20-times greater than the in vivo oxygen
gradient between venous blood and the myocardium. Sea bass do not have a
coronary circulation.
Data analysis and statistics
Myocardial power output (mW g–1 ventricle mass) was
calculated from the product of
[x(Pout–Pin)x
(0.0167 min s–1)]/ventricular mass (g), where
is in ml min–1,
Pout is output pressure and Pin is
input pressure (in Pa). Ventricular mass was determined at the conclusion of
the experiment when the cannulae were checked for correct positioning. The
relationships between cardiac filling pressure and cardiac stroke volume
(VSH) and
(Starling curves), and between Pout and
Pin (power output curves), were derived by fitting curves
to the data for each fish. This permitted an interpolation of values of
VSH, and power
output for standardized levels of filling pressure and output pressure among
fish so that the Starling and power output curves could be based on mean
values derived at each acclimation temperature for six fish (see Figs
2 and
3). Individual fish differed
somewhat in their sensitivity to filling and output pressures and so there are
slight numerical differences for the maximum values presented in the figures
(based on interpolations) and in Table
1 (based on recorded values). Comparisons of the tonic and maximal
effects of adrenaline were performed with a paired t-test. A
probability of less than 5% (P<0.05) was taken as the limit for
statistical significance.
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(12% increase;
Fig. 2A) and power output (15%
increase; Fig. 2C) occurred
with 50–100 nmol l–1 adrenaline. Adrenaline also
shifted the Starling curve to the left
(Fig. 2B), making the heart
more sensitive to filling pressure. As a result, to generate a
VSH of 1.35 ml kg–1, a filling pressure
of only 0.15 kPa was required with 100 nmol l–1 adrenaline
compared with 0.25 kPa with 5 nmol l–1 adrenaline
(Fig. 2B). Most of this shift
in stretch sensitivity was observed between 5 nmol l–1 and 10
nmol l–1 adrenaline.
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(14% increase) occurred with
10–50 nmol l–1 adrenaline
(Fig. 3A) and power output (14%
increase) with 10–50 nmol l–1 adrenaline
(Fig. 3C). Adrenaline also
caused a left-shift in the Starling curve
(Fig. 3B).
The fragility of hearts from 22°C-acclimated sea bass was demonstrated
with two additional heart preparations: one that failed after 10 nmol
l–1 adrenaline and another that failed after 50 nmol
l–1 adrenaline. These hearts initially had an exceptionally
high performance with the tonic adrenaline concentration (maximum
of 158 and 138 ml
min–1 kg–1 and maximum power output of 16
and 19 mW g–1), and thus perhaps we had overtaxed these
hearts. In addition, several experiments were attempted at perfusion
temperatures of 23°C and 24°C, but the hearts performed inconsistently
and poorly.
Comparison of cardiac performance at 18°C and 22°C
Heart rate was significantly higher at 22°C compared with 18°C
although there was no chronotropic effect of adrenaline at either acclimation
temperature. Q10 values for heart rate ranged between 2.27 and
2.63, depending on the adrenaline concentration (calculated from data in
Fig. 1). Maximum power output
was also 27–31% higher for 22°C-acclimated sea bass
(Fig. 1;
Table 1), but this was
primarily because relative ventricular mass was 22% smaller for
22°C-acclimated sea bass (see Materials and methods). However, maximum
was unchanged by temperature
acclimation because maximum VSH was significantly reduced
by 22–24% for 22°C- vs 18°C-acclimated sea bass
(Fig. 1;
Table 1).
The similarity of the Starling response curves for 18°C- and
22°C-acclimated sea bass is illustrated in
Fig. 4. While the curves for
both tonic and maximum stimulation were largely independent of acclimation
temperature, there were two exceptions. The 18°C-acclimated heart
responded to a higher input pressure (producing a significantly higher maximum
VSH) and maximum adrenergic stimulation was produced with
10–50 nmol l–1 adrenaline at 22°C vs
50–100 nmol l–1 adrenaline at 18°C
(Fig. 4). Thus, the relatively
smaller and faster beating 22°C-acclimated sea bass heart had a smaller
maximum VSH and a higher maximum power output, while the
stimulatory effects of adrenaline remained modest (
15% improvements) at
both acclimation temperatures.
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)]
compare favourably with those measured here (95–100
min–1). Likewise, the Q10 of 2.1 reported
(Sandblom et al., 2005) for
in vivo heart rate [51 min–1 at 16°C
(Axelsson et al., 2002)] is
similar to the Q10 values determined here for perfused hearts. This
means that the increase in heart rate (from 80 to 103 min–1)
during swimming (at 2 body lengths s–1) for
22°C-acclimated sea bass is likely through release of vagal tone. Swimming
also increased central venous blood pressure from 0.11 kPa to 0.16 kPa
(Sandblom et al., 2005), a
range that lies well within the filling pressures for the Starling curves
produced here for perfused hearts. Ventral aortic pressure has not been
measured in sea bass, but by assuming a loss of about one third of arterial
blood pressure to gill resistance, the in vivo dorsal aortic blood
pressures of 2.9–3.8 kPa (Sandblom
et al., 2005) can be used to estimate that ventral aortic pressure
would increase from 3.9 kPa to 5.1 kPa during moderate swimming. Again, this
estimate of ventral aortic blood pressure range is well within the output
pressure range used here for the perfused heart. Thus, this limited comparison
suggests that the present data on maximum cardiac performance of the perfused
sea bass heart are highly relevant to the in vivo situation.
The present study also measured the effect of adrenergic stimulation of the
sea bass heart with the aim of comparing maximum cardiac performance with that
of salmonids. This comparison is best done using a common acclimation
temperature across the species, i.e. 18°C. We discovered that maximum
cardiac performance with maximum adrenergic stimulation for
18°C-acclimated sea bass (i.e.
=90.8 and 101.3 ml
min–1 kg–1, and power output=11.4 and 13.2
mW g–1 for tonic and maximum adrenergic stimulation,
respectively) is at least equivalent to if not better than maximum cardiac
performance of rainbow trout and triploid brown trout Salmo trutta.
For 18°C-acclimated triploid brown trout, maximum
and power output reached 118.5 ml
min–1 kg–1 and 12.1 mW g–1,
respectively, with maximum adrenergic stimulation
(Mercier et al., 2002). For
diploid rainbow trout, maximum cardiac performance was lower
[=66–78 ml
min–1 kg–1 and power output=7.0–7.4 mW
g–1 at 15–18°C
(Farrell, 2002)] than the sea
bass. Therefore, the sea bass heart is at least as powerful as the salmonid
heart.
The comparison of cardiac anatomy and physiology between sea bass and
salmonids can be extended a little further with an added caution that unknown
culture effects among species could contribute to differences (see
Gamperl and Farrell, 2004;
Claireaux et al., 2005). At
18°C, heart rate was lower for sea bass (65–70
min–1) when compared with triploid brown trout and rainbow
trout [between 88 and 92 min–1 at 18°C
(Wood et al., 1979;
Altimiras et al., 2002;
Mercier et al., 2002;
Taylor et al., 1996)]. To
compensate, sea bass have up to a 50% larger maximum VSH
(1.4–1.5 ml kg–1) compared with rainbow trout
[0.9–1.1 ml kg–1
(Farrell et al., 1996)] and
triploid brown trout [1.1–1.2 ml kg–1
(Mercier et al., 2002)].
Surprisingly, relative ventricular mass is similar across these three species
at this common acclimation temperature. Given that sea bass lack a coronary
circulation, their entirely spongy myocardium must be more compliant to
accommodate a larger end-diastolic volume and, at the same time, may require a
longer blood residence to extract sufficient oxygen from venous blood. Perhaps
the absence of a coronary circulation necessitates slower heart rates and the
resulting higher maximum VSH compared with salmonids. Of
course, other factors will play a role in settting maximum
VSH since maximum VSH has been shown
to decrease with increases in heart rate and acclimation temperature (present
study) (Farrell et al., 1996).
It has been suggested (Vornanen,
1989) that the negative effect of temperature on cardiac
contractility is directly related to a shortening of the active state of the
cardiomyocyte during the excitation–contraction coupling. In fact, this
negative inotropic effect of temperature may be manifest as the increased
susceptibility of perfused rainbow trout hearts to elevations in output
pressure at high acclimation temperature
(Farrell et al., 1996), a
phenomenon also observed here with sea bass hearts.
Despite the Q10 >2 for heart rate, the present results
clearly suggest that the optimum temperature for maximum performance of the
sea bass heart was reached at the acclimation temperatures of 18 and 22°C.
Maximum was unchanged over this
temperature acclimation range (the increase in heart rate was largely offset
by a decrease in maximum VSH). Maximum power output was
higher at 22°C only as a result of a relatively smaller ventricular mass,
and the heart was more sensitive to a high afterload. This optimum temperature
for maximum cardiac performance in sea bass corresponds well with the optimum
temperatures determined for whole animal functions [active metabolic rate and
aerobic metabolic scope reach a maximum at 22–24°C
(Claireaux and Lagardere,
1999), and 22–24°C is the optimal temperature for growth
(Lefebvre et al., 2001;
Claireaux and Lefrançois, in
press) and endurance swimming
(Claireaux et al., 2006)].
Furthermore, examination of the distribution pattern of sea bass in a
thermally stratified water column shows that sea bass avoid water layers with
a temperature above 22°C (Claireaux
and Lefrançois, in press). The temperature optimum for
maximum cardiac performance in triploid brown trout was found to be between
14°C and 18°C [neither heart rate, maximum power output nor isometric
tension changed significantly (Mercier et
al., 2002)]. Similarly, this temperature range corresponded with a
decrease in aerobic scope during swimming in brown trout
(Altimiras et al., 2002). Thus,
for both sea bass (without a coronary circulation) and salmonids (with a
coronary circulation), there is good correspondence between the temperature
optima for maximum cardiac performance and those for whole animal
functions.
The present study is also consistent with the suggestion that the
temperature optimum for maximum cardiac performance corresponds with a
decreased stimulatory effect of adrenaline
(Farrell et al., 1996). In sea
bass, increasing adrenergic stimulation from a tonic to a maximal level had
modest effects at both acclimation temperatures (no chronotropic effect, only
15% increases in maximum cardiac output and power output, and a left-shift
in the Starling curve without enhancing VSH). Similar
results were obtained with 18°C-acclimated triploid brown trout [a
30–40% increase in maximum and
power output, a modest positive chronotropy, and an attenuation of isometric
tension development in atrial and ventricular strips;
(Mercier et al., 2002)]. Thus,
the relationship between optimum temperature for maximum cardiac performance
and reduced adrenergic stimulation now can be extended beyond salmonids to sea
bass. In reaching this conclusion, we must add a note of caution. The control
condition for comparison was a tonic stimulation with 5 nmol
l–1 adrenaline and although adrenergic effects were modest,
they did occur at the lowest adrenaline concentrations. Future work should
measure plasma catecholamine concentrations and examine the effect of
ß-adrenergic antagonists on cardiac performance.
One factor contributing to reduced adrenergic effects at high acclimation
temperature in salmonids is a reduction in cardiac ß-adrenoceptor density
(Bmax). For rainbow trout, an almost twofold decrease in
Bmax to 20 fmol mg protein–1 and an unchanged
Kd with warm acclimation was reported
(Gamperl et al., 1994),
confirming the earlier finding (Keen et
al., 1993). Gamperl et al. also reported
(Gamperl et al., 1998) a high
Bmax value (58 fmol mg protein–1) for
cold-acclimated chinook salmon (13°C; Oncorhynchus tshawytscha).
However, interspecific differences for Bmax and binding affinity
(Kd) can be considerable among fish species
(Olsson et al., 2000) and
temperature acclimation had no effect on Bmax of the tropical
African catfish Clarias gariepinus, although Kd
increased significantly at an acclimation temperature of 32°C compared
with 15°C and 22°C (Hanson et al.,
2005). Thus, while both Bmax and Kd
of ventricular ß-adrenoceptors can vary with temperature acclimation
within a species, no pattern has emerged across species. In fact, the present
observation that the peak response to adrenaline occurs at a lower
concentration at 22°C than at 18°C can be viewed as either an
increased sensitivity or a constraint on the maximum effect. Consequently, the
role of adrenergic stimulation in setting the optimal performance of salmonid
and non-salmonid fish hearts warrants further attention, especially given the
correspondence between the temperature optima for maximum cardiac performance
and those for whole animal functions.
In summary, the present results clearly show that the sea bass possesses a
powerful heart even though it lacks a coronary circulation. The optimum
acclimation temperature for the sea bass heart appears to be between 18 and
22°C. At these acclimation temperatures maximum adrenergic stimulation has
no effect on either heart rate or maximum
, but has a modest positive inotropic
effect that increases maximum cardiac power output.
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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