Fish Physiology and Biochemistry vol. 13 no. 1 pp 23-30 (1994) Kugler Publications, Amsterdam/New York

Effects of temperature and adrenaline on the atrial myocardium of the cultured Atlantic salmon (Salmo salar) R. Floysand and K.B. Helle Department of Physiology, University of Bergen, Bergen, Norway Accepted: January 5, 1994 Keywords: salmonids, atrial frequency, maximal tension, pD 2 (adrenaline), temperature

Abstract The effects of acute temperature changes (2-17°C) on myocardial contractility with or without adrenergic activation were studied in the isolated spontaneously beating atrium of the Atlantic salmon (Salmo salar) reared at 8°C. The atrial frequency was markedly elevated (from 7 to 46 beats/min) by the rise in temperature from 2-17°C. Both the time to peak tension and to relaxation time were shortened. In contrast, the temperature effect on the maximal tension was modest. Exposure to exogenous adrenaline (1.1 nM- 11 pM) resulted in a substantial enhancement of the maximal tension, notably at 2°C, while potentiation of the frequency at 2, 8 and 14°C, was less pronounced. The apparent affinity (pD 2) for adrenaline on the chronotropy was higher at 8 and 14°C than at 2°C. For the inotropic responses pD 2 was highest at the acclimation temperature (80 C). By comparison with data for the rainbow trout (Oncorhynchusmykiss) obtained by the same experimental design (Ask et al. 1981), species differences were apparent both in temperature dependence of contractile parameters and in their adrenergic activation. The Ql 0 for the frequency in absence of adrenaline was higher in the salmon than in the trout for the temperature interval 2-17°C. The apparent affinities for adrenaline for the frequency at 8°C and 14°C and for the maximal tension responses at 2°C and 8°C were also highest for the salmon atrium.

Introduction Aquaculture in Norwegian coastal waters concentrates on two salmonids, the Atlantic salmon (Salmo salar)and the rainbow trout (Oncorhynchus mykiss), a related species belonging to the Pacific salmon family. Unlike the salmon, the rainbow trout has been successfully cultivated in a wide range of temperatures and salinities around the globe. During coastal farming both salmonids are

commonly exposed to acute changes in water temperature. It is not yet established whether vital organs such as the heart may respond similarly to acute temperature changes in these two species, or whether they respond to stressful stimuli with similar patterns of adrenergic activation of cardiac function over the temperature range relevant for farming conditions. Adrenaline, the dominating circulating catecholamine during physical and environmental distur-

Correspondence to: Dr. Rannfrid Floysand, Department of Physiology, University of Bergen, Arstadveien 19, 5009 Bergen, Norway.

24 bances (stress) in teleosts, may reach high plasma levels in the salmon (500 nM; Floysand et al. 1992) and even higher in the rainbow trout and other species of the Pacific salmon family (up to 1 M: Nakano and Tomlinson, 1967; Mazeaud et al. 1977; Butler et al. 1986; Barton and Iwama 1991; Randall and Perry 1992). In teleosts the catecholamines act as neurotransmitters and circulating hormones and modulates the contractile activity of the teleost heart. Thus, adrenaline has been shown to increase the inotropy and chronotropy in the rainbow trout and other teleosts (Holmgren 1977; Ask et al. 1981; Nilsson 1983; Farrell 1984; Farrell et al. 1986; Graham and Farrell 1989; Vornanen 1989; Farrell and Jones 1992). Similarly, changes in temperature affect the contractile force and frequency of the fish heart (Randall 1970; Ask et al. 1981; Butler and Metcalfe 1983; Farrell 1984; Vornanen 1989). In fish, the heart rate may vary according to species and size (Priede 1983; Farrell and Jones 1992). In the rainbow trout the inotropic effects of adrenaline are more pronounced at low temperature (2°C) during acute temperature changes in vitro, while the chronotropic responses were similar at low and high temperatures (Ask et al. 1981). It is not yet established whether this response pattern also applies to the Atlantic salmon, which is important for interpretations of heart rate measurements as indicators for activation and stress under rearing conditions. The present study aims at a characterization of the intrinsic myocardial properties of the Atlantic salmon, making use of the spontaneously beating atrium as an in vitro model. The properties observed at the acclimation temperature (8°C) were taken as references for the changes obtained by acute temperature changes between 2°C and 17°C. The responses to temperature changes per se and the temperature dependency of the effect of adrenaline on the chronotropic and inotropic responses, have been assessed and compared with previously published data obtained for the rainbow trout myocardium by the same experimental protocol (Ask et al. 1981).

Materials and methods Animals and experimental procedures Cultured Atlantic salmon (Salmo salar), (1-1.5 year old, 0.3-0.6 kg) were obtained from the Institute of Marine Research, Matre Aquaculture Research Station, Norway, and kept for 4 months in a tank with circulating sea water at 8C at the Bergen Aquarium before experiments were begun. The experiments were performed in the autumn. All fish were acclimated to 80 C so the results could be compared to those of rainbow trout acclimated to the same temperature (Ask et al. 1981). All experiments, except for the concentration-response exposure with adrenaline at 14°C, at acute changes of temperature from 8°C, were performed on the same batch of fish. Each fish was killed by a quick blow to the head. The ventral body wall was immediately opened along the midline and the heart was rapidly removed and immersed in oxygenated saline solution, composed essentially as described by Holmes and Stott (1960). The medium contained in mM: NaCl 110, KCI 4.8, CaCl 2 1.5, NaHCO 3 15, NaH 2PO4 2.5, MgSO 4 1.25, glucose 5.6 and was gassed with 9970 02 and 1%7 CO2 throughout the experiment (pH 7.50-7.65 over the temperature range 217°C). It is likely that the majority of the effects reported are due to temperature effects and not due to a concomitant pH change. After removal of the sinus venosus and the ventricle, the spontaneously beating atrium was mounted in a thermostatically controlled organ bath (50 ml) as previously described for the rainbow trout atrium (Ask et al. 1980). Each preparation was given a preload adjusted to maximal force of the spontaneous contractions.

Tension recording The frequency of contractions (beats/min), the maximal tension (Tmax), the times to peak tension (TPT) (0 to 100% force) and maximal relaxation (TR) (100 to 0% force) in each contraction were recorded via a Grass Force Displacement Trans-

25 ducer (type FT 03) and monitored via a Grass Polygraph (model RPS 7D 8A) with Amplifiers (model 7P 122). The parameters were calculated as described by Stene-Larsen (1981). The total tension generated in one minute was quantified as the timetension integral (1 min T dt) recorded by a Grass Polygraph Integrator 7P 10.

Temperature experiments After being mounted in the organ bath the atrium was allowed to equilibrate for 1 h at 8C before onset of experiments. The temperature of the medium was lowered from 8 to 2°C and thereafter increased in steps of 3°C from 2 to 17°C. The preparations were allowed to equilibrate for about 20 min at each temperature.

Adrenergic activation Adrenaline was added in stepwise increasing concentrations at 10 min intervals to cover a concentration range from 1.1 nM to 11.1 rM. One group was examined after 1 h of equilibration in the organ bath at 8°C, identical to the acclimation temperature. Two other groups were equilibrated at 8°C for 45 min before the temperature was lowered to 2°C or increased to 14°C, respectively. At 2 and 14°C the atria were allowed to equilibrate for about 30 min before adrenaline exposure. The concentrations giving half-maximal response were obtained from the concentrationresponse curves at 2, 8 and 14°C to determine the apparent affinity for adrenaline (pD 2 = -log EC 50) (Arians and van Rossum 1957; van Rossum 1963). L-adrenaline bitartrate was obtained from the Norwegian Pharmaceutical Association, NAF.

Statistics Significance of differences (**p < 0.01, *p < 0.05) was calculated by the Wilcoxon rank test for dependent and independent groups. The results are given as means + SEM for (n) atria.

Results Temperature effects on atrialperformance The isolated, spontaneously beating atrium responded to the acute step-wise elevation of temperature with a steep increase in frequency, from 7 beats/min at 20 C to 46 beats/min at 17°C (Table 1), with a Q10 of 3.4 for the whole temperature interval. Within each contraction, the times to peak tension (TPT) and relaxation (TR) were markedly shortened by the acute rise in temperature from 2-17°C, somewhat more pronounced for TPT than for TR (Table 1). The effects of acute temperature changes on the inotropic parameter, the maximal tension (Tma), was on the other hand modest, amounting to a 22% increase from 2 to 17°C (Fig. 1A). The total time tension integral, reflecting the sum of the tension accumulated over a period of 1 min., more than doubled from 2 to 17C (Fig. B), due mainly to the marked positive chronotropic effect of temperature.

Temperature dependence of the adrenalineevoked responses The effects of exogenous adrenaline were examined at three temperatures, 2, 8 and 14°C. The effect of adrenaline on the chronotropic responses revealed a similar, modest potentiation of the frequency at all temperatures (Fig. 2A). The pD 2 values (Table 2) for the chronotropic responses were approximately one order lower at 2°C than at 8 and 14°C, indicating a reduced apparent affinity for adrenaline below the acclimation temperature. Enhanced adrenaline exposure, from 1.1 nM to 3.3 M, was without significant effect on TPT and TR at the three temperatures examined (Table 3). Pronounced inotropic effects of adrenaline were apparent (Fig. 1A, closed symbols), potentiating Tmax 3.5 times at 2°C and 2.5 fold at 8 and 14 0 C. The Tmax responses were significantly higher at 2°C than at 14 0 C (p < 0.01) at adrenaline concentrations at and above 330 nM. In accordance, adrenergic potentiation of the total tension generated/min. was increased 5 fold at 2°C while 2.5 fold

26 Table 1. Effect of temperature on the frequency and the time to peak tension (TPT) and the time for relaxation (TR) in each contraction in the isolated salmon atrium. °C

2 5 8 11 14 17

Frequency (beats/min)

TPT (s)

7.3 15.2 30.1 38.2 43.2 46.3

0.56 0.37 0.28 0.19 0.14 0.11

+ + ± + + +

0.7 2.3 2.3 2.3 2.9 4.7

450 400 -

+ + + + + +

0.01 0.01 0.02 0.01 0.01 0.01

0.74 0.52 0.43 0.40 0.38 0.36

I

350 -

TR (s)

300 -

E

I

I

250 -

+ 0.04 ± 0.02 + 0.02 + 0.01 + 0.01 + 0.01

200150 -

0_a,

100 50 -

Means ± SEM (n = 9) are given for all three parameters.

0-

at 14°C (Fig. 2B). The pD2 value for the Tmax responses was highest at 8°C (Table 2), thus, the apparent affinity for adrenaline peaked at the acclimation temperature.

I

I

I

5

10

Temperature

15

I

20

( C)

600 500

Discussion

I

400 at

The present study demonstrates that the isolated, spontaneously beating atrium of the Atlantic salmon responds with a pronounced rise in frequency of contractions and a modest rise in the maximal tension to acute temperature changes over a temperature range relevant for Norwegian coastal waters. In teleosts the heart rate in vivo is extrinsically governed by sympathetic and parasympathetic pathways and circulating catecholamines (Randall 1970; Farrell and Jones 1992) and the importance of cholinergic and adrenergic modulation varies with temperature (Priede 1974; Wood et al. 1979; De Vera and Priede 1991). Temperature dependent changes in heart rate in teleosts have been attributed to the direct effect of temperature on the pacemaker cells of the heart (Randall 1970). The acclimation temperature has also been demonstrated to affect the frequency responses to acute temperature changes (Bowler and Tirri 1990) and the response to adrenaline (Graham and Farrell 1989). The frequency of contraction in the isolated salmon atrium (Table 1) is close to that reported as a generalized heart rate for teleosts (30 contractions/min at 10°C) (Driedzic and Gesser 1985). By

. EI

X;

300

-_

200 100 0 0

5

10

Temperature

15

20

( C)

Fig. 1. Effect of temperature on the isolated salmon atrium on A (upper) the maximal tension and B (lower) the total tension generated in 1 minute ( l min T dt). The results are calculated in percent of the values obtained at 2°C in the absence of adrenaline (o), (n = 9). The maximal response in the presence of 3.3 AM of adrenaline ( ) are given at 2°C (n = 9), 8°C (n = 11) and 14°C (n =7). Means + SEM are given.

comparison, the rainbow trout atrium (Ask et al. 1981) had, using the same experimental protocol and acclimated to the same temperature (8°C, autumn), a lower in vitro frequency than the salmon atrium. Thus, the high Q1 0 for the frequency in the salmon atrium, notably at the interval 2-8°C (10.6), was in marked contrast to the low Q10 calculated for the rainbow trout atrium (1.6) (Ask et al. 1981).

27 Table 2. The effect of temperature on the apparent potency of adrenaline (pD2 ) on the frequency and maximal tension (Tma,,) of the isolated salmon atrium.

80 70

U

.,, ,

c

ID

60

~

M

\Z

-U-

pD 2 (Adrenaline) -·-

50

-T

Frequency

Tma

6.83 + 0.26 7.58 + 0.191 ]* 7.73 + 0.18 ns

6.99 + 0.10 0.12 * 7.33 6.30 + 0.10 ] **

(n)

0 0 U C

2°C 80 C 14°C

40 V

T,

30

T

(9)

** (11)+ (7)

e

20

Means ± SEM are given for (n) experiments at each temperature. + Values from Fl0ysand and BrAtveit (1993).

U.

10

o

10-9

10-8

10

"

I

I

I

,

-7

10-6

10-5

Adrenoline (M) 650 600 550 500 _g

450 400 350

-.-

-.·

300 250 200 150 100 10-9

10-d

10-7

10-6

10-6

Adrenoline (M) Fig. 2. Effect of adrenaline on the salmon atrium at 2 ( , 8 ( v ) and 14°C ( ). A (upper) Frequency, B (lower) the total tension Illmin T dt). The total time-tension responses have been plotted in percent of the control value (absence of adrenaline) at each temperature. 2C (n=9), 8°C (n= 11) and 14°C (n=7). The difference between the time-tension integral at 2°C and at 14°C was significant at and above 300 nM (p < 0.05). Means + SEM are given.

Therefore, species differences were marked below the acclimation temperature. The time-tension integral showed, on the other hand, similar temperature dependency and was more than doubled in both the salmon (Fig. 1B) and the trout atrium (Ask et al. 1981). A higher intrinsic heart rate more similar to the salmon atrium in vitro has, however, been

demonstrated for the rainbow trout after injection of cholinergic and adrenergic antagonists in both intact fish and in perfused heart preparations at 10-12°C (Farrell 1991). The atrial frequency of contraction and the Tmax although more modest, simultaneously increased with rising temperature from 2 to 17°C in these two salmonids. This is in contrast to the inverse relationship between temperature and Tmax in most other fish species (Helle 1983; Vornanen 1989). In several teleosts, including salmon, the ventricular Tmax increases when the pacing frequency is decreased at a given temperature (Driedzic and Gesser 1985). The effect of acute temperature changes on these responses has, however, not been reported. A pronounced difference was also apparent in the temperature dependence of the atrial TR, but not of TPT, between the salmon and the rainbow trout (Ask et al. 1981). While TR decreased from 1.30s to 1.15s in the trout from 2°C to 17°C, TR in the salmon atrium was shortened from 0.74s to 0.36s over the same temperature interval (Table 1), implying that the time for relaxation were 2 and 3 times faster in the salmon than in the trout atrium at 2°C and at 17°C, respectively. The prime determinant of the relaxation time is the decrease in cytosolic free Ca2 + (Morad and Cleeman 1987; Tibbits et al. 1992). The marked temperature dependent sensitivity of TR in the salmon atrium is consistent with patterns obtained for the isolated atria of several other poikilotherms (Helle 1983), but is in contrast to the modest response in the rainbow trout (Ask et al. 1981). Thus, these results indicate significant differences with respect to Ca 2 + homeostasis between these two salmonids.

28 Table 3. Effect of adrenaline on the time to peak tension (TPT) and the time for relaxation (TR) of the isolated salmon atrium. TPT Adrenaline (nM)

2°C 8°C 14 0C

1.1 0.45+0.02 0.23+0.01 0.14+0.01

3300 0.51 +0.04 0.25+0.01 0.11 +0.02

TR Adrenaline (nM) 1.1 0.52+0.05 0.31+0.01 0.27 ± 0.02

3300 0.62+0.08 0.31+0.01 0.22 +0.02

Means + SEM are given for (n) experiments at each temperature, 2°C (n = 9), 8C (n = 11) and 14°C (n = 7). There was no significant difference between TPT and TR, respectively, at 1. I1and 3300 nM adrenaline at each temperature.

Enhanced exogenous adrenaline was without effect on TPT and TR as parameters for contraction and relaxation in each cycle (Table 3), in keeping with the modest enhancement of the frequency of contraction. The absence of -adrenergic influence on the relaxation in teleosts may be due to the scarcity of myocardial sarcoplasmic reticulum (Vornanen 1989). In the mammalian myocardium, on the other hand, the 3- adrenergic effects are characterized by shortened TPT and TR (Osnes et al. 1985). Our results show that the potentiation by adrenaline on the atrial frequency in the salmon (Fig. 2A) was small compared to the effect of temperatureperse, consistent with observations on the cannulated rainbow trout (Tuurala et al. 1982). The high pD2 values (Table 2) for the salmon atrium speaks, however, against a down-regulation of the receptor population as an explanation for the relative modest potentiating effect of exogenous adrenaline. Adrenaline led, however, to a pronounced inotropic response in the salmon atrium, being larger at 2°C than at 8 and 14°C (Fig. 1A), similar to, but not as marked as in the rainbow trout atrium (Ask et al. 1981). Thus, an enhanced adrenergic effect on Tmax seems apparent in the two salmonids at low temperature. On the other hand, in teleosts ventricular Tmax is found to increase when the pacing frequency is reduced at a given temperature (Driedzic and Gesser 1985), implying a constant time-tension integral at each temperature. In the salmon atrium, however, the time-tension integral was enhanced at 2°C in presence of adrenaline (Fig. B). Further-

more, despite a large difference in frequency between 8C and 2C in the absence of adrenaline (Table 1), the Tmax was similar (Fig. 1A), making an interrelated variation in Tmax and frequency of contraction a less likely explanation for the enhanced adrenergic mediated Tmax at low temperature. By this experimental model, however, we cannot fully exclude that part of the increase in Tmax may be due to the concomitant decrease in frequency. Nevertheless, these in vitro responses may point to a functional role for the circulating adrenaline in adjusting the myocardium to maximal performance at sudden declines in environmental temperature. The frequency of contraction was closely similar in absence (Table 1) and in presence (Fig. 2A) of 1 nM adrenaline at 2°C and at 8C, but not at 14 0 C, at which the frequency was higher in presence of adrenaline. This may reflect differences between atria from different batches of fish, as also reported by Hove-Madsen and Gesser (1989). At high adrenaline concentration (over 1 41 M) the frequency of contraction reached a plateau at 20 C, while at 8 and 14°C the frequency decreased (Fig. 2A). At these concentrations of adrenaline the inotropic responses had not yet reached maximum which may indicate coupling of frequency to Tmax, notably at the higher unphysiological concentrations. Whether this might also reflect a recruitment of inhibitory adrenergic receptor populations or a down-regulation of B3-receptors was not further examined. The importance of circulating catecholamines and adrenergic innervation for regulation of the heart performance during rest and exercise in teleosts is not well established. Both a mainly neuronal (Axelsson et al. 1987) and/or humoral adrenergic tonus have been suggested (Nilsson et al. 1976; Holmgren 1977; Wahlqvist and Nilsson 1977; Nilsson and Axelsson 1988). Graham and Farrell (1989) have postulated that the resting levels of circulating adrenaline (1-9 nM) in the rainbow trout provides a cardiac tonus which may be particularly important at colder temperatures in stimulating the sinoatrial pacemaker. Clear differences were apparent between the two salmonid atria with respect to the affinity for adrenaline and the influence of temperature. The

29 affinity (pD 2 values) for adrenaline was higher for the frequency responses in the salmon (Table 2) than in the trout (Ask et al. 1981) (pD 2; 8°C:6.60 and 14°C: 6.32) both at 8°C (p < 0.01) and 14°C (p < 0.01) and for Tma x at 2C (p < 0.05) and 8°C (p < 0.05) (pD 2; 2C:6.72 and 8C:6.89). These results may indicate a higher affinity for circulating adrenaline in the salmon than in the trout myocardium in vivo. At the acclimation temperature, 8C, the half maximal atrial frequency in vitro was obtained at 60 nM adrenaline (Fig. 2A, Table 2). This adrenaline concentration corresponds to the mean plasma level in salmon under normal rearing conditions in fish pens (Floysand et al. 1992). During handling stress in farmed salmon, plasma adrenaline levels of 200-500 nM were recorded. At similar concentrations in vitro the atrial frequency was maximal. These results therefore indicate a functional importance of the circulating catecholamines on the myocardial performance in the Atlantic salmon both at normal rearing conditions and following stress. In conclusion, this study has demonstrated significant species differences in chronotropic and inotropic responses to acute temperature changes and adrenergic activation of the isolated atrial myocardium between the salmon and the rainbow trout under the same experimental conditions. Assuming that these differences in intrinsic properties also applies to the heart as a whole these findings may have relevance for evaluation and comparison of heart activity in these two salmonids during normal and stressful situations and during sudden changes in environmental temperature in the fish farm pens. Acknowledgements The authors express their sincere gratitude to Dr. scient. John Arne Ask for valuable and helpful advices during the experimental work. Financial support from the Norwegian Fishery Research Council is gratefully acknowledged. References cited AriEns, E.J. and Rossum, J.M. van. 1957. pDx, pA x and pDx values in the analysis of pharmacodynamics. Arch. Int. Pharmacodyn. 110: 275-299.

Ask, J.A., Stene-Larsen, G. and Helle, K.B. 1980. Atrial 52adrenoceptors in the trout. J. Comp. Physiol. 139: 109-115. Ask, J.A., Stene-Larsen, G. and Helle, K.B. 1981. Temperature effects on the 32-adrenoceptors of the trout atrium. J. Comp. Physiol. 143: 161-168. Axelsson, M., Ehrenstr6m, F. and Nilsson, S. 1987. Cholinergic and adrenergic influence on the teleost heart in vivo. Exp. Biol. 46: 179-186. Barton, B.A. and Iwama, G.K. 1991. Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Ann. Rev. Fish Dis. 3-26. Bowler, K. and Tirri, R. 1990. Temperature dependence of the heart isolated from the cold or warm acclimated perch (Perca fluviatilis). Comp. Biochem. Physiol. 96A: 177-180. Butler, P.J. and Metcalfe, J.D. 1983. Control of respiration and circulation. In Control Processes in Fish Physiology. pp. 41-65. Edited by J.C. Rankin, T.J. Pitcher and R.T. Duggan. Croom Helm, Beckenham. Butler, P.J., Metcalfe, J.D. and Ginley, S.A. 1986. Plasma catecholamines in the lesser spotted dogfish and rainbow trout at rest and during different levels of exercise. J. Exp. Biol. 123: 409-421. De Vera, L. and Priede, I.G. 1991. The heart rate variability signal in rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 156: 611-617. 2+ Driedzic, W.R. and Gesser, H. 1985. Ca protection from the negative inotropic effect of contraction frequency on teleost hearts. J. Comp. Physiol. 156B: 135-142. Farrell, A.P. 1984. A review of cardiac performance in the teleost heart: intrinsic and humoral regulation. Can. J. Zool. 62: 523-536. Farrell, A.P. 1991. From hagfish to tuna: A perspective on cardiac function in fish. Physiol. Zool. 64: 1137-1164. Farrell, A.P. and Jones, D.R. 1992. The heart. In Fish Physiology. Vol. XIIA, pp. 1-88. Edited by W.S. Hoar, D.J. Randall and A.P. Farrell. Academic Press, New York. Farrell, A.P., MacLeod, K.R. and Chancey, B. 1986. Intrinsic mechanical properties of the perfused rainbow trout heart and the effects of catecholamines and extracellular calcium under control and acidotic conditions. J. Exp. Biol. 125: 319345. Floysand, R. and Bratveit, M. 1993. Neuronal release of adrenaline by transmural field stimulation of the Atlantic salmon (Salmo salar) cardiac atrium. Comp. Biochem. Physiol. 106C: 205-209. Floysand, R., Ask, J.A., Serck-Hanssen, G. and Helle, K.B. 1992. Plasma catecholamines and accumulation of adrenaline in the atrial cardiac tissue of aquacultured Atlantic salmon (Salmo salar) during stress. J. Fish Biol. 41: 103-111. Graham, M.S. and Farrell, A.P. 1989. The effect of temperature acclimation and adrenaline on the performance of a perfused trout heart. Physiol. Zool. 62: 38-61. Helle, K.B. 1983. Structures of functional interest in the myocardium of lower vertebrates. Comp. Biochem. Physiol. 76A: 447-452. Holmes, W.N. and Stott, G.H. 1960. Studies of the respiration

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Effects of temperature and adrenaline on the atrial myocardium of the cultured Atlantic salmon (Salmo salar).

The effects of acute temperature changes (2-17°C) on myocardial contractility with or without adrenergic activation were studied in the isolated spont...
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