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Division of Comparative Physiology and Biochemistry, Society for Integrative and
Comparative Biology
The Effect of Temperature Acclimation and Adrenaline on the Performance of a Perfused
Trout Heart
Author(s): M. S. Graham and A. P. Farrell
Source: Physiological Zoology, Vol. 62, No. 1 (Jan. - Feb., 1989), pp. 38-61
Published by: The University of Chicago Press. Sponsored by the Division of Comparative
Physiology and Biochemistry, Society for Integrative and Comparative Biology
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38
The
Effect
of
Adrenaline
of a Perfused
Temperature Acclimation
on
the
Trout
and
Performance
Heart
M.S. Graham*
A.P.Farrell
of BiologicalSciences,SimonFraserUniversity,
Department
BritishColumbiaV5A1S6
Burnaby,
Accepted5/24/88
Abstract
Cardiac performance was examined with in situ perfused trout hearts at two acclimation temperatures, 5 C and 15 C. In series I, adrenaline-free perfusion and a
cumulative dose response up to 1 jgmol adrenaline - L-' was examined. In series II,
tonic adrenergic stimulation (5 nmol . L-) and a cumulative dose response up to
50 nmol - L-1 was examined Tonic adrenergic stimulation was importantfor chronotropic and inotropic stability, especially at5 C. Heart rate and maximum cardiac
output were significantly higher at 15 C than at5 C. Maximum stroke volume at5
C was the same as or greater than the maximum stroke volume at 15 C Adrenergic
stimulation produced quantitatively differentpositive chronotropic and inotropic
effects at both temperatures andpartially compensatedfor the direct efect of temperature; the chronic Q.o valuesfor heart rate and maximum cardiac output were
1.30-1.40. Trout acclimated to 5 C had a relatively larger ventricle mass, which
permitted a higher absolute stroke work at 5 C than at 15 C
Introduction
When faced with a change in watertemperature,fish can either compensate
for the temperaturechange, conform to it, or avoid the thermal effects by
modifying their behavior (Precht 1958). In terms of cardiacfunction, temperaturedirectly affects the intrinsic properties of the heart and indirectly
affectscardiacfunction throughtemperature-relatedmodificationsto extrinsic controls (Randall 1970; Seibert 1979; Wood, Pieprzak,and Trott 1979;
* Current
3X8Canada.
British
P.O.Box3232,Vancouver,
address:
Vancouver
Public
Columbia,
V6B
Aquarium,
ofChicago.
1989.C 1989byTheUniversity
Zoology
Physiological
62(1):38-61.
Allrights
reserved.
0031-935X/89/6201-87112$02.00
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Acclimation
intheTrout
Heart 39
Temperature
TABLE1
Morphometric and biologic information
ExperimentalSeries
Total Body
Mass(g)
Ventricle
Mass(g)
Ventricle:
Body-Mass Sex Ratio
Ratio(%)
(M:F)
622
.64a
.103a
(14.2)
(.040)
(.0051)
561
(18.6)
.44b
.078b
(.046)
(.0055)
596
.70a
.117
(40.8)
(.096)
(.0146)
531
(34.8)
.42b
(.031)
.078b
(.0025)
8:1
485
.38b
.070b
3:1
(53.9)
(.085)
(.0081)
Series I
(5 C, N= 11)
10:1
Series I
(15 C, N= 7)
Series II
(5 C, N= 6)
Series II
(15 C, N= 9)
Time trials
(15 C, N= 4)
4:3
5:1
Note.Allvaluesexceptthosefor"Ventricle:Body-Mass
Ratio"aremeans(SEM)forN
animalsin eachseries.Significant
differences(P < .05)forventriclemassand
experimental
ratioareindicatedbymeanvalueshavinga differentlettersuperscript.
ventricle:body-mass
Farrell1984). While the direct effects of temperaturetend to suppress cardiac activity (negative chronotropyand inotropy), adrenergic stimulation
tends to increase cardiac activity (positive chronotropyand inotropy). In
view of these antagonisticactions, we examined whether adrenergicstimulation of the heartwas an importantmechanismto compensate for the direct
effects of temperature.
Adrenaline is found in the blood of resting trout (Butler, Metcalfe, and
McGinley1986; Primmettet al. 1986;Milliganand Wood 1987) and is more
effective than noradrenalineas a cardiacstimulant (Nilsson 1981, 1983;Ask
1983;Farrell,MacLeod,and Chancey 1986). Withstressfulexercise, plasma
adrenalinelevels rise from 1-5 nmol - L-1to 35-50 nmol - L-1in trout(Primmett et al. 1986; Milliganand Wood 1987). Physicalperturbations(e.g., tail
grabbing) increase adrenaline levels to as high as 1 glmol L-' (Nakano
L
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40 M.S. Graham
andA.P.Farrell
and Tomlinson 1967; Butler et al. 1986). Adrenalinelevels of 1 jLmol- L-1
produced maximalstimulationof perfused troutheartsat 10 C (Farrellet al.
1986). We comparedcardiacfunction with and without adrenergicstimulation to provide informationboth on the importanceof tonic adrenergicstimulation by the catecholamines normally found in the blood of resting fish
and on the role of elevated blood catecholamines in stressed trout.
An additional effect of temperatureis to significantlychange the blood
viscosity of fish (Grahamand Fletcher 1984). Viscositydirectlyaffectsvascular resistance and therefore the amount of work performed by the heart to
pump blood (Farrell 1984). This problem is compounded by the direct
effect of temperatureon cardiacinotropy.Relativeheartweight increases in
cold-acclimated trout (Farrell 1987; Farrell,Johansen, and Graham1988),
goldfish (Tsukuda, Liu, and Fujii 1986), carp (Goolish 1987), and catfish
(J. D. Kentand C. L. Prosser,personal communication). Thus, the increase
in ventricle muscle mass could compensate for reduced inotropy and increased blood viscosity.We tested this hypothesis here.
A working perfused heart was used to separate the direct and indirect
effects of temperatureon the overall pumping ability of the heart (Graham
and Farrell1985; Farrellet al. 1986). An advantageoffered by this approach
is that chronotropic effects (intrinsic heart rhythm) and inotropic effects
(maximumstrokevolume and pressuredevelopment) can be assessed with
the same heartpreparation.The present studyused troutacclimatedto 5 and
15 C, and their in situ cardiac performancewas assessed as a function of
acclimation temperatureand adrenergic stimulation. Chronic Q10values
were derived for comparisons.
andMethods
Material
Animals
Rainbowtrout (Salmo gairdneri) were purchasedfroma local fishfarmhaving water temperaturesof 7-10 C year round. The fish were acclimated for
at least 4 wk in 2,000-Ltankssupplied with flowing, dechlorinatedtapwater.
The mean acclimation temperatureduring the winter months was 5.5 C
(SEM = 0.1 C); fish acclimated to this temperaturewere used for experiments at 5 C. Meanacclimationtemperatureduringthe summermonthswas
15.5 C (SEM = 1.9 C); fish acclimated to this temperaturewere used for
experiments at 15 C. The light-darkcycle for each time of year was maintained according to informationfrom the VancouverInternationalAirport
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intheTrout
Acclimation
Heart41
Temperature
(49"N latitude). Fish were fed commercial Fish Chow ad lib. five times per
week. Pertinentmorphometricdataare found in table 1.
Heart Preparation
The procedurefor the in situ trout-heartpreparationfollowed thatdescribed
elsewhere (Farrellet al. 1986), except thatthe temperatureof the perfusate
going to the heart and the water for irrigatingthe gills approximatedthe
experimental temperature.Preliminaryexperiments indicated that this approach significantlyreduced the experimental equilibration time. During
surgerythere was minimal interruptionof flow to the heart and no direct
physical manipulationof the heart.The input cannulato the heartwas introduced into the sinus venosus through a hepatic vein, and saline perfusion
was begun immediately. Silk thread was used to secure the input cannula
and to occlude the remaininghepatic veins. Separatesilk ligatureswere tied
tightly around each ductus Cuvierto occlude these veins and to crush the
cardiacbranchesof the vagus nerve. Smallerveins to the sinus venosus were
not individuallytied off, but backflowinto small vessels was negligible (Farrell et al. 1986). The output cannulawas secured in the ventralaortavia an
incision in the ventralbody wall. Preparationtime was 10-15 min.
Forthe experiment the fish was fully immersed in a pH-adjusted(pH 7.9)
Cortlandsaline baththatwas constantlyaerated.The input cannulareceived
perfusate from a constant-pressurereservoir that was water jacketed. The
output cannulawas connected to a pressurehead, and an in-line flow probe
was placed in the output tubing near to the cannula.The input and output
pressureswere measuredthrough saline-filled sidearmsconnected to pressure transducers.The perfusate going to the heart contained the following per liter: CaC12- 2H20 0.37 g, NaCl 7.25 g, KCl 0.23 g, dextrose 1 g,
MgSO4 - 7H20 0.23 g, NaH2PO4 - H20 0.014 g, and Na2HPO40.33 g. The
perfusatewas equilibratedwith a 0.5%/99.5%CO2/airmixture (PacificMedigas Ltd., Vancouver), and pH was brought to 7.9 after the addition of
NaHCO3(1 g - L-'). The temperaturesof both the perfusateand the experimental chamberwere controlled at 5 C or 15 C with a thermostatedwater
bath. Eachheartwas tested at the acclimationtemperatureonly.
Heart rate in the in situ preparation was set by the intrinsic pacemaker
rhythm (Farrell et al. 1986) and did not normally vary significantly under
control conditions. Consequently, cardiac output (Q) was varied by altering
stroke volume of the heart (SVH). SVHwas easily controlled by raising or
lowering the height of the input-pressure head. The diastolic output pressure was varied by adjusting the height of the output-pressure head.
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42 M.S. Graham
andA.P.Farrell
701
Fig. 1. An example of data
recorded during a cardiovascular work challenge.
Stable control conditions
were establishedprior to
the flow challenge. For the
flow challenge, the input-
Output
Pressure
cmH20O50
Input
Pressure
05-,
cmH2O
1 min
Cardiac
20
Output
mL min-l kg-1
pressure reservoir was
raised while the outputpressure head was unchanged. Raising the inputpressure increased stroke volume and thus cardiac output. Inputpressure was raised until there was no further increase
in stroke volume, and the associated cardiac output was termed "maximum cardiac output. " The change in inputpressure had no significant
effect on heart rate. Inputpressure was lowered to restore the control cardiac outputprior to the pressure challenge. For the pressure challenge, the
output-pressure head was first lowered and then raised in a stepwisefashion. Since inputpressure and heart rate were constant during the pressure
challenge, any measured changes in cardiac output were a result of the
change in outputpressure. Typically, lowering the outputpressureproduced a modest increase in cardiac output, while raising outputpressure
compromised cardiac output. Excessive outputpressures could stop cardiac output entirely (table 1).
o-
IFlow Challengef
I
Pressure Challenge
Experimental Protocols
ControlCardiac Performance.Aftercompleting the surgery,each heartwas
allowed to equilibrateto the experimentaltemperaturefor 5-20 min while
it performed a control level of cardiacperformance.Stable heart rate (fH)
and temperaturemeasurementsnearthe heartwere used to establish equilibration. Control Q was set at 10 mL - min-'1 kg-' at 5 C and at 20 mL
min-'1 kg-1 at 15 C. Restingcardiacoutput in troutis 17 mL- min-' - kg-1L
at 11 C (KiceniukandJones 1977). Controlmean outputpressurewas set at
50 cm H20 independent of temperature.Ventralaortic blood pressure in
resting troutis 47-54 cm H20 (KiceniukandJones 1977).
Cardiac WorkChallenge. To profile maximum cardiacperformance,each
heart was presented with the same experimental work challenge. Cardiac
work was increased in two ways: first,by increasing SVHto a maximum in
orderto increaseflowwork,and, second, by raisingthe diastolic outputpressure to increase pressure work (fig. 1). The work challenge took approxi-
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Acclimation
intheTrout
Heart43
Temperature
TABLE
2
Effectof increasing outputpressure on theperfused heart at 5 C (N = 11)
OutputPressure
Adreneline Concentration
73 cm H20
85 cm H20
Adrenalinefree
1 nmol - L-1.
10 nmol . L-1............
100 nmol - L-1
1 mol. L-1..........
7
8
9
10
11
1
3
9
8
10
Note.Eachheartwasbrieflyexposedto eachpressure.Thenumberof preparations
ableto
concentration.
generateflowat73 and85 cmH20is indicatedasa functionof adrenaline
mately 10 min to complete. The control level of cardiacperformancewas
restored before each subsequent experimental perturbation,and a further
5-min equilibrationwas allowed before the work challenge was repeated.
Withthe diastolic output pressure constant,input pressurewas increased
at a rate of 0.04-0.14 cm H20 - s-1 over 30-60 s until SVHdid not increase
further.This was termed maximum SVH,and the associated Q was termed
maximum Q. Control Q was restored after a stable level of maximum Q
was recorded. Positive inotropic effects were indicated by an increase in
maximum Q and/or a lower input pressure to generate the maximum Q
(i.e., an increasedsensitivityto filling pressure).
The relative stability of control Q as a function of output pressure was
also used as a measure of inotropic performance.Since increasing output
pressure ultimately compromised Q, positive inotropy was indicated by
maintenance of control Q at a higher output pressure. To test this, input
pressure was set to produce control Q, and mean output pressure was first
lowered to 35-40 cm H20 and then increased in a stepwise fashion to 7375 cm H20 without changing input pressure. Outputpressurewas variedby
adjustingthe height of the output-pressurehead. Qwas monitored throughout. All preparationscould generate an outflowat outputpressuresof 73-75
cm H20, but only some could generate an outflowat higher pressures (table
2). Therefore,a pressureof -73-75 cm H20 was adopted as a point of comparisonfor maximumpressuredevelopment.
Effectof Adrenaline. Adrenergic effects were studied at 5 C and 15 C by
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44 M.S. Graham
andA.P.Farrell
using two experimental series. Adrenaline (=epinephrine HCl, Sigma, St.
Louis) was used in all experiments. Freshadrenalinewas added to the perfusate just before the startof each test. Photodegradationof adrenalinewas
limited by covering the perfusatecontainerswith foil.
Experimentalseries I comparedmaximumcardiacperformancewith and
without adrenaline in the perfusate (up to 1 gmol adrenaline - L-'). By the
time fHhad stabilized in the experimental chamber, the hearts had been
perfused with adrenaline-freesaline for at least 30 min (including surgery
time). Therefore, it was assumed that the cardiacperformancemeasuredat
this time had minimal adrenergic influence. Cardiacperformancewas first
measured with adrenaline-freeperfusion by using the work challenge and
then was reexamined for a cumulativelog concentrationrangeof adrenaline
(1 nmol - L-', 10 nmol . L-', 100 nmol - L-, and 1 gmol - L-'). The heart
was allowed to equilibratefor 5 min at each adrenalineconcentrationbefore
performingthe work challenges. These experiments lasted --100 min.
Experimental series II compared maximum cardiac performance with
adrenaline concentrations of 5 nmol - L-1, 10 nmol
.
L-', and 50 nmol
-'
in a manneridentical to thatof series I, except thatthere was no adrenalinefree perfusion. The heart received perfusate containing 5 nmol adrenaline - L-1 during surgery.This initial adrenaline concentrationwas established in partbecause adrenaline-freeperfusion at 5 C in series I produced
slow and irregularrhythms (no beats for up to 4 s) and an unusually poor
response to filling pressurein manypreparations,which were consequently
discarded. (Irregularheartbeatswere rare at 15 C in series I.) Preliminary
experiments indicated thatthe presence of 5 nmol adrenaline - L-1(but not
of 1 nmol adrenaline - L-') in the initial perfusateprevented these arrhythmias at 5 C. The experiments in series II lasted --60 min.
Since an adrenalineconcentrationof 5 nmol . L-' is similarto thatfound
in resting trout,comparisonsof cardiacperformanceat 5 nmol adrenaline
L-1'in series II with adrenaline-freeperfusion in series I provided a means
to evaluate the role of tonic adrenergic stimulation of the heart by bloodborne catecholamines. Furthermore,since the maximum adrenaline concentrationused in series II (50 nmol - L-1)is similarto the elevated plasma
levels observed after stressful exercise in trout, comparisons can be made
with series I, where there was maximalstimulationof the heartwith 1 p1mol
adrenaline
.
L-7.
Time Trials.The time-trialexperimentswere designed to assess anydeterioration of cardiacperformancewith time. The protocol was similar to that
used in series I in thatthe work challenge was repeated five times consecu-
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intheTrout
Acclimation
Heart45
Temperature
tively but with no adrenaline present. The time trials could only be performed at 15 C because prolonged exposure to adrenaline-freeperfusion at
5 C resulted in cardiac arrhythmias.These experiments typically lasted
80 min.
Measurementsand Calculations
The input pressureto the sinus venosus and the output pressure in the ventralaorta,immediatelyanteriorto the bulbus arteriosus,were measuredcontinuously. Pressuresignals (LDI-5;Narco Telecare, Houston) were amplified appropriatelybefore being displayed on a chartrecorder (Gould 2400;
Gould, Ohio). The resistancesof the output and input cannulaewere determined with known flow rates of perfusate,and all pressure measurements
were corrected accordingly. Outflow was measured continuously with an
in-line electromagnetic flow probe (SWF-4;Zepada Instruments,Seattle)
placed in the outputtubing immediatelyafterthe outputcannula.Meanflow
values were recorded. The flow probe was calibratedwith known flow rates
of perfusate.Representative10-s samples of the analogue pressureand flow
signals were converted to digital signals and stored on computer disk for
subsequent analysis (Farrell and Bruce 1987). Cardiacoutput was determined as the productof SVHand fHand was expressed in mL - min-' - kg-1
(where kg refers to the total wet mass of the fish). Mass-specificpower output of the heartwas calculated as (Q X [outputpressure - input pressure]
X 0.00163)/g and was in units of mW/g (where g refersto the totalwet mass
of the ventricle). To assess the importanceof ventricle size on cardiacpower
output, absolute power output and absolute stroke work were also calculated. Absolutepower output (mW) = (mass-specificpower output) X (ventricle mass), and absolute stroke work (mJ) = (absolute power output)/
(heartrate/60).
StatisticalProcedures
Repeated-measuresanalysis of variancewas used to compare mean values.
Unpairedt-testswere used to compare mean values between temperatures.
Statisticalprocedures were performed using the packages available on the
IBMmainframecomputerat Simon FraserUniversity.Significantdifferences
were at the 95%confidence level.
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46 M.S. Graham
andA.P.Farrell
Results
Time Trials
The cardiovascularvariablesassociatedwith control and maximumQ conditions are presented in table 3 for each of the five consecutive work challenges, the entire series lasting --80 min. In the firsttrial with adrenalinefree perfusion,raisinginputpressureby 2.5 cm H20 approximatelydoubled
SVH, Q, and power output without a significantchange in fH;fH decreased
with subsequent adrenaline-freeperfusion such that, in the second trial,
control fHwas reduced by 14%,and, in the thirdtrial,control fHwas reduced
by a further4%.ControlfHwas unchanged duringthe fourthand fifthtrials.
The significantdecrease in fHbetween the firstand second trials required
that, in order to maintain control Q, input pressure be raised to increase
control SVH.
MaximumSVH,Q, and power output were not significantlydifferentbetween the firstand second trials.There was a trendtowarda lower maximum
SVH,a result that, coupled with the trend towarda higher input pressure to
stimulatemaximumSVH,suggests thatthere was a minor inotropic deteriorationby the fifthtrial.The net effect of this chronotropicand inotropicdeteriorationwas that maximumQ and power output were reduced by 10%for
the second trial and by 16%,19%,and 21%for the third, fourth, and fifth
trials, respectively. The initial decrease in fHwas the majorreason for the
changes. The time-dependent change in fHwas importantin interpreting
datain series I.
Series I
ControlConditions.Withthe adrenaline-freeperfusion (table 4), the intrinsic fHwas significantlyhigherat 15 C thanat 5 C. Thus,control SVHwas made
similarat both experimentaltemperaturesso thatthe control Q at 15 C was
set to twice that at 5 C. A similar input pressure was used at both temperatures to produce the control SVH.
Adrenalineproducedpositive chronotropiceffectsat 5 C andat 15 C (table
4). Comparedwith adrenaline-freeperfusion, 1 jimol adrenaline . L-1produced a significant increase in fH at both experimental temperatures (14.4
beats . min-1 at 5 C and 11.6 beats . min-1 at 15 C). In addition, comparison
of fHfor the time trials (table 3) and series I (table 4) indicates that a concentration of adrenaline >1 nmol L-1 offset the initial chronotropic deterioration seen with adrenaline-free perfusion in the time trials. If the lower concentrations of adrenaline had not affected fH, there should have been a sig-
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letter
g-1)
(.40)4.07b
(.72)
(.48)3.90c
(.63)
5.02abc
Maximum
4.52(.41)4.22a
(mW.
superscript
Power Control
2.50(.30)
2.63(.30)2.44(.31)2.57(.23)2.82(.38)
same
the
kg-1)
having
.
(3.93)
(2.68)
(2.99)
(3.96)
Maximum
34.6b
42.4abc
38.6(3.69)
35.8a
32.9c
min-1
-
column
each
Q (mL Control20.2(.62)21.2(.63)19.6(.95)21.1(1.02)
23.1(1.68)
within
Values
kg-1) Maximum
.69 (.089)
.63 (.073)
.70 (.080)
.68 (.071)
.62 (.074) min.
15
(mL
about
39a(.037)
.32abcd
(.028)
.39C
(.021)
.37b(.032)
SVH Control
.43d(.032)
experiments
trial
min-1)Maximum
(5.1)
(4.3)
(3.9)55.7c
53.6b
(3.3)
(2.6)
63.1abcd
56.2a
53.5d
time-trial
the
in
(beats.
fH
(5.1)
(4.8)
(4.0)53.8c
Control
(4.1)
(4.5)
56.2a
54.0b
53.8d
64.2abcd
(SEM).
means
Maximum
2.57(.62)
2.46(.65)
2.46(.52)2.51(.35)3.03(.50)
represent
Control.11 (.24).10 (.21).12 (.19).31 (.20)
.68 (.60)
and
C
15
for
different
are
cardiacPressure
H20)
(cm
Input
maximum
and
1
Control
TABLE
Each
4.
N=
output
3
lasted
2
3
4
5
Trial Trial Trial Trial Trial
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values
Allsignificantly
0.05).
(P<
Note.
were
C
15
(.098)
(.11)2.04*
(.54)
(.12)
(.098)
2.10*
2.04*
2.07*
2.06*
marked
g-1)
C
(mW. 5
Power
.87 (.031)
.84 (.050)
.80 (.049)
.78 (.062)
.82 (.054)
between
adrenaline
*
kg-')
-
C
15
(.54)19.47*
(.58)19.10*
(.50)19.35
(.68)19.15*
(.36)
19.46*
0.05)
each
<
(P
within
9.87(.41)
9.61(.49)10.13
(.31)10.84
(.27)
(.34)10.35
groups
differences
min-1
C
Q (mL 5
C
kg-') 15
.
.29a(.015)
.37 (.033)
.35 (.029)
.39 (.029)
.35a(.018)
C
SVH 5
.27a(.011)
.33(.026)
.44 (.044)
.48 (.058)
.43a(.042)
C
15
(3.07)
(4.36)
(3.84)
(3.02)
(3.73)
53.6*
57.1*
68.7d,*
57.12*a
50.8*
min-1)
-
and
C
5
at
C
fH (beats 5
C
15
Pressure
H20)
experiments
I
C
(cm 5
Input
and
C,indicates
(.076) 5
.040',*
.16 (.12)
.42a(.21).23 (.12).21 (.14)
for
11
asterisk
N=
.46 (.11).31a(.096)
.54a(.12)
.66 (.15).43 (.12)
for
free
values
L-1
L-1
.
L-1
L-'......
nmol
nmol
100
1
Concentration
Adrenaline 10
Adrenaline
(SEM).
superscript
A
means
letter.
are
same
Values
the
nmol
Control
TABLE
0.05)
<
(P
superscripts
Lettered
difference
C.
15
for
(1.02) 7 significant
(3.11)
25.8(2.93)
33.3(2.29)
23.1(3.25)
40.3a
25.9a
a
N=
Series
4
significant
temperature
indicate
between
(mL
C
15
trial.
values
jmol
1
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Note.
with
intheTrout
Acclimation
Heart 49
Temperature
nificantdecrease in fH,similarto thatseen with adrenaline-freeperfusion in
the time trials.This was not the case. With 10 nmol adrenaline - L-1,fHwas
the same as the initial condition at 5 C and was only 6%lower at 15 C (table
4). By comparison,fHwas reduced by 18%during the third time trial with
adrenaline-freeperfusion (table 3).
Because 1 pmol adrenaline - L-1produced a tachycardia,input pressure
was lowered to significantlyreduce control SVuand to set the control Q.
Althoughcontrol SVHwith 1 pmol adrenaline - L-1was comparableat both
experimental temperatures,input pressure was significantlylower at 15 C
comparedwith 5 C (table 4). There was no significantdifference between
input pressuresat 5 C and at 15 C for other adrenalineconcentrationsor for
adrenaline-freeperfusion. This indicates that the perfused trout heartwas
more sensitive to filling pressureat 15 C in the presence of high adrenaline
concentrations.
Flowand PressureChallenges.Forthe 5 C and 15 C experiments,the cardiovasculardata for maximum Q conditions at various adrenaline concentrations are presented in table 5. Withadrenaline-freeperfusion, raising input
pressureby 3 cm H20 produced a maximumQ thatwas approximatelytwice
the control Q. Comparedwith adrenaline-freeperfusion, maximumQ with
1 jmol adrenaline - L-' was increased by 62%at 5 C and by 25%at 15 C.
There was a significantadrenergicstimulation of fHand maximumSVHat 5
C but a significantincrease only in fHat 15 C (table 5). Even though maximum SVHwas unchangedat 15 C with adrenergicstimulation,1 pmol adrenaline . L-' increased the sensitivity of the heart to input pressure, as indicated by a significantlylower input pressure associated with maximumSVH
(table 5).
The pressurework challenge revealed that 1 pmol adrenaline . L-' had a
positive inotropic effect at both experimental temperatures.With adrenaline-free perfusion, raising the output pressure above 70 cm H20 reduced
Q by 17%at both experimental temperatures(figs. 2A, 2B). At 5 C, 1 .tmol
adrenaline - L-' completely prevented this decrease in Q (fig. 2A) and also
permitted flow at output pressures up to 85 cm H20 (table 2). At 15 C, the
inotropic effect of 1 pmol adrenaline L-1was effective at maintainingQ at
elevated output pressures, although it was not as effective at doing so as it
was at 5 C.
Series II
Control Comparisonsbetween series I and series II clearly demonstrated
the importanceof tonic adrenergicstimulationwith an adrenalineconcen-
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C
15
(.25)
(.25)3.49*
(.26)4.02*
(.31)4.93a*
(.31)
3.90a*
3.62*
C
(mW. 5
Power
(.16)1.71(.16)1.93(.19)2.50(.15)2.88a
1.76a
(.10)
g-1)
*
experiments
I
min-1-
C
15
(1.97)
(2.29)
(2.39)
(3.22)
(3.16)
39.50*
34.33*
38.38a,*
47.23a,*
35.73
table
in
as
-
Series
C
Q (mLkg-1) 5
Cfor
15
4.
(1.80)
(1.62)
(2.06)
(1.56)
(1.40)
22.06
24.98
31.12a
35.98b
22.30ab
indicated
C
kg-') 15
and
C
5
at
are
.71 (.055)
.74 (.044)
.70 (.033)
.69 (.035)
.72 (.032)
0.05)
(P<
(mL
C
SVH 5
(.031)
.92d(.037)
.90b(.034)
.95c(.034)
.81a(.042)
.75abcd
differences
conditions
flow
C
15
min-')
(2.56) Significant
(2.74)
(3.86)
(4.24)
54.2*
53.9a.*
51.4(3.54)
50.1*
67.7a'*
C.
15
C
fH (beats 5
maximum
C
15
during
*
(1.20)
(2.31)
28.0(2.31)
32.9(1.66)
39.3a
30.0a
27.7(2.19)
N=
(.38)
2.26*
3.53(.66)3.49(.50)3.13(.43)3.10(.61)
and
C,
5
for
11
H20)
C
(cm 5
Input
Pressure
for
7
3.57(.34)3.75(.28)4.18(.29)3.09(.25)3.28(.28)
N=
(SEM).
valuesproduced
free
5
L-1
-
L-l
-
L-1
-
means
L-1
are
-
nmol
nmol
Mmol
nmol
100 1
1
10
Cardiovascular Adrenaline
Concentration
TABLE
Adrenaline
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All use subject to JSTOR Terms and Conditions
Values
Note.
Acclimation
intheTrout
Heart51
Temperature
A
2.0
30
C
2.0-
0
5030 70
-2.0
70
-2.0-
03
2.0-
2.00
30
70
70
So
I
-4.0-
,~
-2.0
-2.0-
Seriesll- 50C
N-6
-4.0-
Output
Pressure,
SeriesTl-15C
N.9
cmH20
Fig. 2. Thepressure challenge produced changes in the resting cardiac output (Q). The change in resting Q (AQ) ispresented as afunction of the
outputpressure for the various adrenaline concentrations tested in series I
and series II. Symbols represent thefollowing adrenaline concentrations:
series I, O = 1 mol - L-', 9 = 100 nmol L- A = 10 nmol L-', E = 1
nmol L-, 0 = adrenaline-free; series II, A = 50 nmol . L-J, A = 10
nmol - L-', * = 5 nmol - L-1. For series I:panelA, N = 11 (5 C);panel B, C,
N = 7 (15 C). For series II:panel C, B, N = 6 (5 C); panel D, N = 9 (15 C).
Allpoints are means, and vertical bars represent SEM.
trationsimilar to that found in the plasma of resting trout. Initial perfusion
with 5 nmol adrenaline - L-1in series II completely prevented the arrhythmicity and time-dependent decrease in fHthatwere associatedwith adrenaline-free perfusion at 5 C in series I.
As in series I, fHin series II was significantlygreaterat 15 C than at 5 C at
all adrenalineconcentrations(table 6). At 5 C the initialfHat 5 nmol adrenaline - L-1 (table 6) was significantlygreaterthan that with adrenaline-free
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C
15
2.16(.11)
2.16(.12)2.14(.08) 3.80(.18)
(.18)
(.22)
4.08b
4.58b
g-l)
C
(mW. 5
Power
.87
.81
.83
(.070) (.063) (.070) 2.38(.19)2.38(.19)2.58(.17)
output
cardiac
of
level
the
to
kg-1') C
15
(.54) (.60) (.29)
20.14*20.06* 20.22
(2.10)
(2.86) refer
(2.04)
35.56*
39.39b,*
44.58b,*
min-1'
C
15
C
Q (mL 5
and
C
5
at
II)
C
kg-1) 15
.
"maximum"
(.38) (.16) (.38)
10.64 9.98 10.17
(2.87)
(2.89)
(3.03)
30.42
31.00
33.17
and
.43 (.032)
.41a(.025)
.37a(.014) .77(.035)
.81 (.035)
.82 (.036) "Control"
(mL
C
(Series
SVH 5
C
15
min-1)
adrenaline
of
C
fH (beats. 5
levels
C
15
Pressure
H20)
tophysiological C
(cm 5
Input
.30 (.031)
.30 (.036)
.26 (.030) .83 (.074)
.82 (.056)
.85 (.059) experiments.
C 4.
15
*
fortable
a*
9 in
as
(3.0)
(1.7) 48.4(3.0)
(1.6)54.4b,*
(1.6) N=
48.5*
49.8(2.1)55.8a'*
48.9b,*
36.7(3.1)35.5(3.3)40.4(3.1) 37.2(2.7)
36.8(1.9)39.2(2.5)
*
.31
.19* .18*
(.12) (.10) (.14) 2.33(.61)
(.35)2.13*
(.27)
2.46*
.
.68
.74
.70
(.21) (.16) (.13) 3.23(.25)
3.96(.49)3.29(.28)
and
indicated
are
0.05)
experiments,
C
5 (P<
for
6
N=
differences
(SEM).
response
L-1
L-1
-
L-1
L-1
-
L-1
L-1
.
6
nmol nmol
nmol nmol
nmol
nmol
10
10
5
5
50
50
Cardiovascular
Concentration
Control:
TABLE
Maximum:
Adrenaline
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All use subject to JSTOR Terms and Conditions
Significant
means
are
values
experiment.
All
each
Note.
in
Acclimation
intheTrout
Heart53
Temperature
perfusion in series I (table 4). In addition, the fHat 50 nmol adrenaline L-' in series II was not significantlydifferentfrom the fHat 1 Ilmol adrenaline - L-1in series I. This comparisonemphasizes the importanceof tonic
adrenergicstimulationof fHat 5 C. Comparedwith the 5-nmol - L- adrenaline concentration, both the 10- and 50-nmol - L-1adrenaline concentrations significantlyincreased fHat 15 C but not at 5 C (table 6).
Flow and Pressure Challenge. Raising input pressure had no significant
effect on fHat either experimental temperature(table 6). MaximumQ was
significantlygreaterat 15 C thanat 5 C, which reflecteda significantlyhigher
fH at 15 C (table 6). Comparedwith the 5-nmol - L-' adrenaline concentration, both the 10- and 50-nmol - L-Uadrenaline concentrations increased
maximum Q significantlyat 15 C but not 5 C. Comparedwith the 100- and
1-pmol - L-1adrenaline concentrationsin series I (table 5), the 50-nmol L-' adrenaline concentration in series II (table 6) did not show a significantlydifferentmaximumQat either experimentaltemperature.
The positive inotropic effect of adrenalinewas qualitativelyand quantitatively similar to that in series I. Adrenergicstimulationincreased the sensitivity of the heart to filling pressure at 15 C but not at 5 C, since the input
pressure required to generate control SVHand maximum SVHwas significantly lower at 15 C than at 5 C (table 6). Furthermore,when the output
pressurewas increasedto - 70 cm H20, 50 nmol adrenaline L-1prevented
a significantdecrease in Q at 5 C (fig. 2C); at 15 C 50 nmol adrenaline - L-I
partiallyoffset the decrease in Q (fig. 2D).
Chronic Q1c Values. The positive chronotropic and inotropic effects of
adrenaline were qualitativelysimilar for perfused hearts from trout acclimated to 5 C and 15 C. However, there were quantitativedifferences,which
were apparentwhen Qiovalues were compared.
The QO0for fHwas 2.20 with adrenaline-freeperfusion; 1 jtmol adrenaline - L-1 reduced this Qo0to 1.70 in series I, and in series II the Q10for fH
was 1.38 with 50 nmol adrenaline - L-'. Adrenergic stimulation therefore
clearly compensated for the direct effect of temperatureon the intrinsicfH,.
This compensation was also reflected in the maximumQ.The Qio for maximum Q was 1.72 with adrenaline-freeperfusion; 1 jimol adrenaline L-I
reduced this Q10to 1.31 in series I, and in series II the Q10was 1.34 at 50
nmol adrenaline L-1.
Heart Size. Heart mass was significantly larger in cold-acclimated trout (table 1). Relative ventricle mass (expressed as a percentage of body mass)
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54 M.S. Graham
andA.P.Farrell
was --50% greaterin 5 C-acclimatedtrout.The importanceof this increase
in ventricle mass on cardiac performancewas seen in two ways: first, by
comparing the maximum values for absolute power output and mass-specific power output and, second, by comparing absolute stroke work of the
heartat the two experimentaltemperatures.
The Q10of 1.78 for the maximum value of mass-specificpower output
indicated that there was little temperaturecompensation per gram of muscle. However,the Qo0for absolute power outputwas 1.34 and indicatedthat
the increase in ventricle mass provides partialcompensation for the direct
effect of temperatureon inotropy.A similar conclusion was reached when
absolute strokeworkwas calculated.Maximumstrokeworkwas consistently
greaterin cold-acclimatedhearts (rangingfrom 2.25 mJ to 2.81 mJ) than in
warm-acclimatedhearts (rangingfrom 1.12 mJto 2.12 mJ) (calculatedfrom
datain tables 1, 5, 6). Thus, the work per beat of the relativelylargerhearts
in cold-acclimated trout can exceed that in the hearts of warm-acclimated
trout,although the warm-acclimatedtroutheartcan beat faster.
Discussion
Adrenergic Stimulation
In these experiments we studied the effects of adrenaline, even though
adrenaline and noradrenalineare found in similar concentrations in the
blood and heart tissue/nerve endings at rest (Abrahamssonand Nilsson
1978; Pennec and LeBras1984). The selection of adrenalineas the sole adrenergic agonist was based on the fact thatadrenalineis generally 10 times
more effective than noradrenaline in stimulating P-adrenoceptorsin the
troutheart (Ask, Stene-Larsen,and Helle 1981; Farrellet al. 1986). Furthermore, following stressful exercise, adrenaline is the dominant hormone in
trout (Nilsson 1983), although noradrenalineis the dominant neurotransmitterreleased into perfusatefollowing vagal stimulationof perfused goldfish hearts(Cameronand O'Connor1979).
The present study demonstratedin several ways that the resting level of
circulatingcatecholamines (1-9 nmol - L-1;Woodward1982;Axelsson and
Nilsson 1986; Primmettet al. 1986; Milligan and Wood 1987) provides an
important, if not essential, cardiac tonus in trout. First, the time-trial experiments at 15 C showed initial chronotropic and then progressive inotropic
deterioration with adrenaline-free perfusion. Second, preparations were discarded because they became arrhythmic and unresponsive to filling pressure
at 5 C with adrenaline-free perfusion. Even with hearts that were relatively
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intheTrout
Heart55
Acclimation
Temperature
stable at 5 C, adrenaline-freeperfusion could not be prolonged much beyond 30 min without deterioration.Third,in series II, initial perfusionwith
5 nmol adrenaline - L-1prevented these chronotropicand inotropic problems at 5 C.
The importanceof adrenalinefor successful perfusion of isolated and in
situ trout hearts has been noted elsewhere (Bennion 1968; Farrellet al.
1986). There are several indications that the tonic effect of adrenaline at
colder temperaturesmay be particularlyimportantin stimulatingthe sinoatrialpacemakerand in preventingatrioventriculardesynchronization.Bennion (1968) used 300 nmol adrenaline - L-1to preventthe weak contraction
and atrioventricularblock associatedwith adrenaline-freeperfusion,but she
made no distinctionbetween the adrenergiceffect at 6 C and at 15 C. Farrell
et al. (1986) found that only four of 75 in situ heart preparationsshowed
serious arrhythmiasat 10 C with initial adrenaline-free perfusion; subsequent perfusion with >10 nmol adrenaline - L-1prevented arrhythmia.In
the present study, arrhythmiawas frequent at 5 C but was absent at 15 C.
Adrenergiceffects on atrioventricularconduction were also reportedat 8 C
for the eel (Anguilla anguilla). In the eel, a-adrenoceptorswere stimulated
at adrenaline concentrations>5 jimol - L-1to produce desynchronization
(Pennec and Peyraud1983). However, the adrenergiceffects in the eel are
clearly the opposite of those found in the trout both in terms of the effect
and in terms of the type of adrenoceptor involved. (Positive inotropy and
chronotropyare mediated by P-adrenoceptors[Asket al. 1981;Cameronand
Brown 1981; Farrellet al. 1986; Temma et al. 1986] without involvement
of a-adrenoceptorsin trout [Salmogairdneri], goldfish [Carassiusauratus],
carp [Cyprinuscarpio], and flounder [Pleuronectesplatessa] but not perch
[Percafluviatilus][Tirriand Lehto 1984].)
The present study also found that the progressive inotropic deterioration
associated with adrenaline-freeperfusion was ameliorated by adrenaline.
This phenomenon may be related to-but not necessarily limited to-the
absence of adrenergicstimulationof metabolism, adrenergicstimulationof
transsarcolemmalcalcium movement, or progressive atrialoverdistension.
Atrialoverdistension was observed in isolated trout hearts during adrenaline-free perfusion (A. P. Farrell,unpublished observation)and was amelioratedby adrenaline.However,atrialoverdistension may not be a concern in
intacttrout,in which the atriumis constrainedwithin the pericardium(Farrell et al. 1988).
Although the present study established the importanceof tonic humoral
stimulationof the heart under resting conditions, there is normallya complex interplaybetween excitatoryadrenergictonus and inhibitorycholiner-
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andA.P.Farrell
56 M.S. Graham
gic (vagal) tonus in intact teleosts under resting conditions (Axelsson,
Ehrenstrom,and Nilsson 1987). Adrenergicstimulation of the fish heart is
possible throughthree mechanisms:circulatingcatecholamines,adrenergic
innervation,and cells containingcatecholamines.Adrenergicnerves,which
enter the sinus venosus through cardiacbranches of the vagus nerve, converge on the sinoatrialplexus (pacemaker) and to some extent along the
atrialcanaland the atrioventricularfunnel (Laurent,Holmgren,and Nilsson
1983). Also, adrenergicinnervationis associated with the coronaryvasculature (Holmgren 1977) and so is more dense in the compact myocardium
(Yamauchiand Burnstock1968). In addition to storage in nerve terminals,
Yamauchiand Burnstock (1968) demonstrated the presence of catecholamines in granularvesicles in the sarcoplasmof the troutheart.Since nothing is known about the levels of catecholamines released from storage
granules or nerve terminals, the results of the present study apply only to
adrenergic stimulation of the heart through blood-borne catecholamines.
The adrenaline concentrationsused here were within physiological limits,
although the maximumlevel used in series I (1 pmol - L-) should be considered representativeonly of plasmalevels of troutundergoingsevere handling stress.
Adrenaline levels similar to those associated with stressful exercise produced positive inotropic and chronotropic effects at 15 C (series II) that
were comparable with those previously observed both at 10 C for in situ
perfused hearts (Farrellet al. 1986) and at various temperaturesfor atrial
strips (Asket al. 1981). At 5 C, inotropicand chronotropiceffects of adrenaline were limited to those produced by tonic stimulation. This finding is
consistent with the previous observationthatadrenergicstimulationof fHis
reduced in troutacclimatedto 5 C (Wood et al. 1979). In contrast,adrenergic stimulation of maximumtension was three times greaterat 2 C than at
14 C in atrialstrips taken from troutacclimatedto 8 C and tested at 2 C and
at 14 C (Asket al. 1981). This greaterinotropiceffect of adrenalineat a lower
temperaturecontrastswith the present results and may reflect a difference
between an acute temperaturechange and temperatureacclimation.
Temperature Effects
The present study revealed direct and indirect effects of temperature on cardiac performance. Maximum Q was apparently affected more by temperature-dependent changes in fHthan it was by temperature-dependent effects
on inotropy. An increase in heart mass with cold acclimation and differences
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Acclimation
intheTrout
Heart57
Temperature
in adrenergicstimulationpartiallycompensated for the direct effects of temperatureon the intrinsicmechanicalpropertiesof the troutheart.
The direct effect of temperatureon fHhas been well documented by experiments involving acute temperaturechanges. In general, the acute Q10
for fHis --2.0 for isolated hearts and for intact fish. For goldfish hearts in
vitro, the Q0ofor fHwas 2.0 and 1.6 for acclimation temperaturesof 25 and
10 C, respectively (Tsukudaet al. 1986). For isolated trout hearts, the Q10
for fHwas 2.4 (Bennion 1968). In perfused sea ravenhearts (Hemitripterus
americanus), Q0ofor fHwas 1.9 and 1.4 for acclimation temperatures of 5 C
and 15 C, respectively (Graham and Farrell 1985). The Q1ofor fHwas 1.76
for intact trout (Hughes and Roberts1970), 2.6 for intact carp (Moffittand
Crawshaw1983), 2.1-2.5 for intact winter flounder (Pseudopleuronectes
americanus) (Cech et al. 1976), and 1.78-2.78 for the intact eel (Seibert
1979). Thus, it appearsunlikely that there is little compensation of resting
fH in intactfish duringan acute temperaturechange.
In contrast,chronic temperaturechanges are accompanied by a compensation of resting fH in intact fish. The Q1ovalues for fH derived from intact
fish acclimated to different temperatureswere generally <2.0 (1.5 for the
trout[Priede1974],2.6 for the trout[Woodet al. 1979],1.2 for the eel [Seibert
1979], and 1.3-1.6 for winter flounder [Cech et al. 1976]). Most evidence
suggests that this temperaturecompensation involves extrinsic modulation
ratherthan the pacemakerper se. Forexample, the Q10for fHwas increased
to 2.0 in intactfish afteradrenergicor cholinergic modulationof fHwas surgically or pharmacologicallyblocked (Priede 1974; Siebert 1979;Wood et al.
1979). Similarly,with adrenaline-freeperfusion in vitro, the Q0ofor fHwas
2.2 for the trout (present study), 2.0 for the sea raven (Grahamand Farrell
1985), and 1.7 for the eel (Tsukudaet al. 1986), and in the present study
adrenergicstimulationsignificantlyreduced the Q0ofor fHfrom 2.20 to 1.38.
Modulationof cholinergic inhibition of fHis also importantduringtemperature acclimation and has been considered elsewhere (Priede 1974; Siebert
1979;Wood et al. 1979).
Although many studies have provided informationon how temperature
acclimation affects fH, little is known concerning temperatureeffects on
SVH.The present study is the firstto compare the regulationof SVHin coldand warm-acclimatedtrout. SVHis influenced by the volume of the heart
chambers, filling pressure, filling time, and the inotropic state of the heart
(Randall 1970; Farrell 1984). The cold-acclimated trout heart was generally
less sensitive to filling pressure in the presence of adrenaline (tables 5, 6).
This probably reflects a direct effect of temperature, since the perfused sea
raven heart responded similarly to an acute, as well as to a chronic, tempera-
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58 M.S. Graham
andA.P.Farrell
ture change (Grahamand Farrell1985). Nevertheless, maximumSVHof the
heartwas the same or greaterin cold-acclimatedcomparedwith warm-acclimated trout. This is an importantfinding because it implies that cole and
warm-acclimatedtroutare equally capable of exploiting the maximumvolume of the heartchambers,provided thatthere is adequateadrenergicstimulation and thatthere is no limitationon venous returnpressure.
Perhapsthe most importantcompensationfor the directeffect of temperature on inotropy was the --50% increase in relative ventricle mass; an increase in the number of contractileunits in the ventricle compensated for
the relativelyweaker contractionof individualunits, as indicatedby the fact
thatabsolute strokework was higher in cold-acclimatedthan in warm-acclimated trout hearts.The consequence of increasing the relative heart mass
in cold-acclimatedtroutwas veryclear.The chronic Q1ofor maximumQ was
-1.34 despite temperature-relateddifferences in fH.This Qo0representsa
--66% compensation.
An increase in relative heart mass during cold acclimation has been reported elsewhere for a variety of teleosts, including trout (Tsukudaet al.
1986; Farrell 1987; Goolish 1987; Farrellet al. 1988;J. D. Kent and C. L.
Prosser, personal communication). While muscle protein increased with
these increases in heart mass, cardiac growth in trout involves significant
myocyte hyperplasiaas well as myocyte hypertrophy(Farrellet al. 1988). It
is not clear at this time which of these two mechanisms operates in trout
during temperatureacclimation. However, it does seem likely that an increase in heartmass may be a general mechanismfor temperatureconipensation among teleosts.
The present observationsand conclusions regardingthe effectof temperature on SVHseem consistent with those of previous studies on intact fish.
Winter flounder increase resting Q by increasing both SVHand fHduring
temperatureacclimation (Cech et al. 1976), whereas increases in fHare the
primarymeans of increasing resting Q during acute temperaturechanges
(Stevens et al. 1972;Cech et al. 1976). In addition, Priede (1974) calculated
that, during swimming, SVHincreased more than twofold in both 6 C- and
15 C-acclimated trout, which is consistent with our suggestion that maximum SVHis not compromised at low watertemperatures.
In summary,the present study indicates that resting levels of circulating
catecholamines probablyimpartan importantcardiactonus in intact trout.
At 5 C this tonus appearedto be more importantin preservingcardiacrhythmicity, while at 15 C it stimulatedinotropyto a greaterdegree. There was a
direct effect of temperatureon fH,which affectedmaximumQ and was partially compensated by tonic adrenergicstimulation.Because maximumSV,
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intheTrout
Acclimation
Heart59
Temperature
was unaffectedby temperature,there was a 66%compensation of maximum
Q. Ventriculargrowth,stimulatedduringseasonal cold acclimation,contributed directly to maintainingmaximum SVHand stroke work in cold-acclimated trout.These compensations may be importantin maintaininga high
level of cardiacperformance-and hence of swimming performance--during winter months.
Acknowledgments
JeffJohansen is thankedfor his technical assistance,especially with the statistical analysis. This study was funded by the NaturalSciences and Engineering Council of Canadathrough an operating grant to A. P. Farrelland
by a postdoctoralfellowship to M. S. Graham.
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