Cardiac preload and venous return in swimming sea bass (Dicentrarchus labrax L.)
1 Department of Zoology, Göteborg University, Box 463, S-405 30
Göteborg, Sweden
2 Faculty of Agricultural Sciences and Department of Zoology, University of
British Columbia, Vancouver, BC, V6T 1Z4, Canada
3 Department of Biology, Institute of Physics and Measurement Technology,
Linköpings Universitet, S-58183 Linköping, Sweden
4 Centre de Recherche sur les Ecosystèmes Marins et Aquacoles
(CNRS-IFREMER), Place du Séminaire, F-17137, L'Houmeau,
France
* Author for correspondence (e-mail: erik.sandblom{at}zool.gu.se)
Accepted 15 March 2005
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: cardiac preload, cardiac output, exercise, heart rate, mean circulatory filling pressure, prazosin, sea bass, stroke volume, teleost, venous capacitance, venous return
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
This line of logic ignores the fact that under steady-state conditions,
equals venous return and the heart
can pump only what it gets back from the venous circulation. Moreover, any
increase in PCV during exercise will reduce the pressure
gradient for venous return (flow) to the heart from the venous periphery, if
end-capillary blood pressure and venous resistance remain unaltered. Thus, in
addition to increasing cardiac filling pressure, a proportional increase in
peripheral venous pressure is expected to ensure that venous return can match
the increase in
. Venous return can be
estimated from measurements of PCV and venular blood
pressures.
The mean circulatory filling pressure (MCFP) is an index of venous
capacitance. It is measured as the venous pressure after a short (5-10 s)
cardiac arrest and also represents the upstream venous (venular) pressure that
drives venous return (Pang,
2001; Rothe, 1986
,
1993
;
Sandblom and Axelsson, 2005
).
MCFP can increase due to an increased smooth muscle tone and/or a decreased
compliance in venous capacitance vessels
(Conklin et al., 1997
;
Hoagland et al., 2000
;
Olson et al., 1997
;
Pang, 2001
; Rothe,
1986
,
1993
;
Zhang et al., 1998
). While
comprehensive studies have examined the nervous and humoral control of venous
capacitance in unaesthetized fish under resting conditions
(Conklin et al., 1997
;
Hoagland et al., 2000
;
Olson et al., 1997
;
Sandblom and Axelsson, 2005
;
Zhang et al., 1998
), none have
considered the changes in venous capacitance that are likely to occur during
exercise. Furthermore, basic information on PCV during
exercise is limited to a few studies and what data exist are compromised by
noisy signals and/or experiments on a small number of animals
(Jones and Randall, 1978
;
Kiceniuk and Jones, 1977
;
Stevens and Randall,
1967
).
The primary objective of this study was therefore to measure changes in
PCV and MCFP in a fast swimming teleost, the European sea
bass (Dicentrarchus labrax L.). By combining PCV
and MCFP measurements, it was also possible to assess the degree to which the
pressure gradient for venous return, venous capacitance and cardiac preload
change during the periods of increased
associated with exercise. Also, the
role of
-adrenoceptor control of these responses was examined, since
Zhang et al. (1998
) identified
that venous capacitance in resting rainbow trout (Oncorhynchus
mykiss) can be altered by
-adrenergic mechanisms.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Surgical procedures
Prior to surgery the fish were anaesthetized in seawater containing MS-222
(approx 100 mg l-1) and placed on water-soaked foam on a surgery
table. During surgery, the fish was covered with wet tissue paper and the
gills were continuously irrigated with aerated, chilled (11-16°C)
seawater containing MS-222 (
50 mg l-1). The ventral aorta was
exposed with an incision on the right side of the isthmus and dissected free.
A Perspex cuff-type 20 MHz Doppler flow probe (Iowa Doppler products; Iowa
City, IA, USA), with an inner diameter of 1.8-2.0 mm, was positioned around
the aorta proximal to the bulbus to measure relative changes in
(Fig. 1). Also, a cuff-type
vascular occluder (i.d. 2.5-4.3 mm) was positioned posterior to the flow probe
to obtain zero-flow during measurement of MCFP. The occluder was constructed
from Perspex, a heat-flared water-filled PE-50 catheter and a piece of latex
rubber (model Thin, Dental Dam, Coltène/Whaledent Inc, USA and Canada).
The rubber was tied with a 4-0 suture around the flared end of the PE tubing
(Fig. 1). The sinus venosus was
non-occlusively cannulated to measure PCV
(Altimiras and Axelsson, 2004
).
Briefly, the operculum was retracted and the left lateral part of the ductus
of Cuvier was carefully exposed and dissected free with an incision between
the cleithrum and the fifth branchial arch. A small portion of the vessel wall
was lifted with forceps and secured with a 4-0 suture, allowing the vessel to
be gently lifted during the cannulation procedure. This procedure prevents
blood loss, and is an improvement on the method used by Farrell and Clutterham
(2003
). A PE-50 catheter, with
2-3 side-holes to keep it patent and a bubble 1 cm from the tip, was inserted
into the ductus of Cuvier through a small incision made close to the suture
holding the vessel. A 4-0 suture was used to close the vessel wall around the
catheter, leaving the bubble located on the luminal side of the vessel wall.
The catheter was secured with silk sutures to the skin. The third efferent
branchial artery on the left side was occlusively cannulated to measure dorsal
aortic pressure (PDA). To do this, the first two gill
arches were retracted to expose the third gill arch, which was gently
retracted. The branchial artery was dissected free close to the angle of the
branchial arch, occluded upstream with a 4-0 silk suture and cannulated
downstream with a tapered PE-50 catheter
(Fig. 1). The catheter was
secured with 3-0 silk sutures around the gill arch and secured to the skin
with 3-0 silk sutures. The catheters and the lead from the flow probe were
collectively secured with a 3-0 suture to the back of the fish. Both blood
pressure catheters were filled with physiological saline (0.9% NaCl).
Following surgery, the fish were revived in fresh seawater, placed in plastic
floating tubes in the holding tanks and allowed a 24 h recovery before
experiments commenced.
|
Experimental protocol
A stainless steel, Brett-type swimtunnel respirometer was used in the
present study. This tunnel had been designed to exercise individual fish in a
non-turbulent water flow with a uniform cross-sectional water velocity. The
total water volume was 48 l and the swim chamber had a square cross-sectional
area of 290 cm2. A propeller downstream of the swim chamber
generated water flow. The flow in the swimtunnel was calibrated
(Marsh-McBirney 200 flow meter; Frederick, MD, USA) in cm s-1,
which was converted to swimming speeds in body lengths s-1
(BL s-1). The respirometer was thermostatted by immersion
in a large outer stainless steel tank that received a flow of aerated water.
Since venous pressure is low readings can be affected by any changes in the
pressure head on the propeller in the swim-channel when water velocity is
changed. To minimise this problem the lid to the swim chamber was removed.
Water pressure was measured with a saline-filled catheter immersed in the
channel, and no pressure fluctuations were observed at the swimming speeds
used (up to 2 BL s-1). The swim channel was covered with
an opaque black plastic sheet to avoid visual disturbance of the fish.
All experiments were conducted at a temperature of 22°C. The
experimental protocol started with a 2 min recording at rest, i.e., the fish
oriented into a low water velocity and maintaining position without swimming.
MCFP was measured at rest by occluding the ventral aorta for 8 s. Water
velocity was then gradually increased over a 5 min period until the fish
reached a swimming speed of 1 BL s-1, which was maintained
for 15 min. MCFP was remeasured at the end of this period. The same procedure
was used for a swimming speed of 2 BL s-1. Water velocity
was then reduced to the resting condition over a 2 min period and an
-adrenoceptor antagonist (prazosin, 1 mg kg-1
Mb; Pfizer, Sandwich, UK) was administered via
the venous catheter. The entire protocol was repeated 1.5-2.0 h later.
Preliminary experiments had revealed that an exercise period of 15 min was
well beyond the time necessary to establish stable cardiovascular measurements
in untreated fish.
Successful ventral aortic occlusion always resulted in a rapid fall in PDA, a rise in PCV and a complete cessation of ventral aortic flow (Fig. 2). Although the ventral aorta was easily accessible, the vessel proved to be relatively fragile as compared with rainbow trout and several sea bass died due to fatal rupture of the ventral aorta during occlusion. This generally occurred after the first occlusion and might have been due to mechanical abrasion from the vascular occluder during recovery. Another unusual finding was the low occurrence of blood clotting in the catheters during routine surgery and this was the reason why heparin was omitted from the saline.
|
Data acquisition, calculations and statistical analysis
Both blood pressure catheters were connected to pressure transducers (model
DPT-6100, pvb Medizintechnik, Kirchseeon, Germany), calibrated against a
static water column with the water surface of the swim channel serving as the
zero reference pressure. The signals from the pressure transducers were
amplified with a 4ChAmp amplifier (Somedic, Hörby, Sweden). Relative
cardiac output () was recorded with a
directional-pulsed Doppler flow meter (model 545C-4, University of Iowa, USA).
The digital signals were fed into a portable computer running a custom made
program, General Acquisition (Labview version 6.01, National Instruments,
Austin, TX, USA).
Heart rate (fH) was obtained from either pulsatile
pressure or flow records. Relative changes in cardiac stroke volume
(Vs) were calculated as
/fH. Total
systemic resistance (Rsys) was calculated from the
pressure drop in the circulation divided by cardiac output
Rsys=(PDA-PCV)/
.
For the Vs,
and
Rsys calculations raw data was used and the initial
untreated resting value for each fish was arbitrarily set to 100%. The plateau
pressure in PCV during ventral aortic occlusion was
assumed to equal mean circulatory filling pressure (MCFP), and the average
pressure between the 5th and 7th seconds of ventral aortic occlusion is
reported here. This time interval is sufficient to obtain reasonably steady
plateau values, while minimising the compromising effects of barostatic
reflexes (Sandblom and Axelsson,
2005
). A similar method has been used previously to measure MCFP
in the trout (Hoagland et al.,
2000
; Zhang et al.,
1998
). No correction for inequalities in blood remaining in the
arterial circulation after occlusion was performed, because the difference was
assumed to be negligible due to the large differences in compliances and
volumes of the arterial and the venous compartments
(Rothe, 1993
;
Zhang et al., 1998
). The
pressure gradient (
PV) for venous return was
calculated as
![]() | (1) |
Resistance to venous return (Rv) was calculated as
![]() | (2) |
assuming that equals venous
return.
Data (mean values ±S.E.M.) are
presented only for fish that performed steady state swimming at both water
velocities. Partial data from fish that exhibited either erratic swimming
behaviours, burst swimming, died after prazosin treatment, lost a catheter, or
the ventral aorta ruptured were discarded. Cardiovascular data were taken from
the last 90 s of each exercise period. For the calculations of venous
variables, i.e. Fig. 4,
PCV was taken as the average of a 30 s period before
ventral aortic occlusion. Wilcoxon matched pairs signed-ranks test, with a
fiduciary level of P0.05 was used to evaluate statistically
significant differences in cardiovascular variables at different swimming
speeds and between treatments. To compensate for multiple two-group
comparisons, a modified Bonferroni-test was applied
(Holm, 1979
).
|
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
Fig. 4 shows the rise in
PCV during exercise and illustrates changes in venous
variables during exercise. In addition to an increase in
PCV with increased swimming speed, MCFP increased
significantly (0.27±0.02 kPa at rest to 0.31±0.02 kPa and
0.40±0.04 kPa, respectively). Because the rise in MCFP was
proportionally larger than that in PCV,
PV increased significantly from 0.16±0.01
kPa at rest to 0.18±0.02 kPa at 1 BL s-1 and
0.24±0.02 kPa at 2 BL s-1, whereas
Rv remained unchanged.
Effects of -adrenoceptor blockade on cardiovascular performance during swimming
Blockade of -adrenergic receptors with prazosin showed that the
cardiovascular system is at least partially controlled via
-adrenoceptors, both at rest as well as during exercise (Figs
3 and
4). At rest, prazosin treatment
significantly decreased Rsys, producing a significant
arterial hypotension while PCV increased
significantly.
During swimming after prazosin treatment, the increases in
PCV and fH were absent at 1
BL s-1, but not at 2 BL s-1. In fact,
the increase in PCV was accentuated significantly at 2
BL s-1 after prazosin. Prazosin also significantly
accentuated the decrease in Rsys at 2 BL
s-1 (from the resting value of 85.7±3.2 to 73.5±3.6%)
and the corresponding hypotension (PDA from 2.9±0.1
to 2.5±0.1 kPa). Again, Vs remained unchanged
throughout the swim challenges after prazosin treatment despite the increase
in PCV (Fig.
3). After prazosin, MCFP also remained unaltered at 1 BL
s-1, but increased significantly from 0.28±0.02 kPa at rest
to 0.40±0.05 kPa during swimming at 2 BL s-1, but
no more so than before prazosin treatment
(Fig. 4). As a result
PV increased significantly compared with the
resting value at 2 BL s-1, although this response was not
as pronounced as pre-prazosin treatment. Rv remained
unaltered throughout the experiment (Fig.
4).
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Hemodynamics of venous return and cardiac filling pressure in sea bass
The present study is the first to demonstrate an active control of the
venous vasculature during exercise in any species of fish. Very few studies
have successfully measured cardiac filling pressure during swimming in teleost
fish. Kiceniuk and Jones
(1977) found that
PCV in the common cardinal vein of four rainbow trout
increased significantly during swimming only when the fish swam at critical
swimming speed (Ucrit), and not at intermediate swimming
speeds. This finding is surprising because Vs increased
significantly at intermediate swimming speeds, suggesting that these increases
in Vs were not a result of increased filling pressure. It
is likely that increased adrenergic stimulation of the heart, which is known
to both increase during swimming (Axelsson,
1988
) and increase the sensitivity of the heart to filling
pressure (Farrell et al.,
1986
) permitted these increases in Vs without
a concomittent increase in PCV. Stevens and Randall
(1967
) measured venous
pressure and flow in the subintestinal vein (= hepatic portal vein), and found
that venous pressure increased whereas flow decreased. Since the hepatic
portal vein drains the gastrointestinal tract and is located upstream of the
liver, and arterial gut blood flow decreases during exercise
(Axelsson et al., 1989
;
Axelsson and Fritsche, 1991
;
Farrell et al., 2001
;
Thorarensen et al., 1993
), it
is uncertain to what extent these changes directly affected cardiac
performance (for further discussion, see
Jones and Randall, 1978
).
In the present study, and
fH increased during swimming. The increase in
fH would have reduced cardiac filling time, but it is
clear that the observed increase in preload would have compensated for this,
leaving Vs unchanged. As pointed out in the introduction,
the increase in PCV in itself could decrease the pressure
gradient driving venous return from the periphery to the heart. However, a
proportionally larger increase in MCFP ensured that the pressure gradient for
venous return actually increased and since Rv was
unchanged, venous return would be increased to support the increase in
(Fig. 4).
The increase in MCFP could be attributed to either an increased venous
tone, a decreased venous compliance or a combination of both
(Conklin et al., 1997;
Hoagland et al., 2000
;
Olson et al., 1997
;
Pang, 2001
; Rothe,
1986
,
1993
;
Zhang et al., 1998
). In
rainbow trout, adrenaline increases venous tone through an
-adrenergic
control and decreases venous compliance
(Sandblom and Axelsson, 2005
;
Zhang et al., 1998
). Since
vascular capacitance curves could not be constructed in the present study, we
do not know the exact mechanism for the increase in MCFP. Nevertheless, the
observation that the increases in MCFP, PCV,
,
PV and
fH during swimming at 1 BL s-1 were
abolished after
-adrenoceptor blockade (Figs
3 and
4), suggests an important
-adrenergic control mechanism for the venous vasculature in sea bass
during exercise, which can mobilize venous blood towards the heart and
increase cardiac preload. This control mechanism was evident in resting fish
as well. About 2 h after prazosin treatment, resting cardiovascular variables
in the sea bass were significantly altered (Figs
3 and
4); PCV
increased and both Rsys and PDA
decreased. It is unlikely that this increase in PCV was
mediated by either an increased transcapillary fluid uptake, thus increasing
blood volume, or an up-regulation of some compensatory vasoactive system since
this would have affected MCFP as well. The importance of an
-adrenergic
tone on the arterial side of the circulation has been previously demonstated
at rest and during swimming in other fish species
(Axelsson and Fritsche, 1991
;
Axelsson and Nilsson, 1986
;
Smith, 1978
), and was
confirmed here because after prazosin treatment sea bass could not maintain
Rsys at 2 BL s-1 and suffered a major
systemic hypotension. In view of this, it could be argued that the increase in
PCV was only a consequence of the reduction in
Rsys, but then MCFP would not have increased. Instead, the
accentuated reduction in arterial pressure at 2 BL s-1
possibly triggered the activation of some unknown vasoactive system, acting
primarily on the venous vasculature. One concern with the present study is
that an increased adrenergic tone on resistance vessels may have counteracted
a further decrease in Rsys during exercise and resulted in
an unaltered resistance in untreated fish. It is unknown whether the
adrenergic control of MCFP is mediated by adrenergic nerves and/or circulating
catecholamines. In cod (Axelsson and
Nilsson, 1986
; Butler et al.,
1989
; Smith et al.,
1985
) and trout (Smith,
1978
) it has been demonstrated that the increase in arterial blood
pressure observed during moderate exercise is exclusively mediated by
adrenergic nerves. Whether the same is true for the venous circulation in fish
is not yet known.
A possible consequence of a decreased venous capacitance, manifested as the
increase in MCFP, is that blood volume from the venous compartment is
redistributed to other parts of the circulation, such as muscle capillary
beds, respiratory organs and central veins
(Pang, 2001). It is possible
that much of the blood redistributed from the venous system in the sea bass
during exercise, in addition to increasing cardiac preload, served to fill
gill vasculature and muscle capillary beds. In mammals the splanchnic
circulation has a high capacitance and is the primary reservoir for blood
volume mobilization during exercise (Pang,
2001
; Rothe,
1986
). To what extent splanchnic venous blood volume is mobilized
during exercise in fish is unclear, even though Stevens and Randall
(1967
) demonstrated that blood
flow in the subintestinal vein (e.g. portal vein) decreased and venous
pressure increased in rainbow trout. Albeit somewhat meager evidence, the
observations are consistent with blood volume mobilization from the splanchnic
venous compartment during exercise in fish. As judged from the drop in
PDA and Rsys during swimming at 2
BL s-1 after prazosin, it is possible that the gut
circulation continued to be perfused (unlike the normal decrease with
exercise) as perfusion of locomotory muscles increased
(Axelsson and Fritsche, 1991
;
Axelsson et al., 2000
;
Farrell et al., 2001
;
Thorarensen et al., 1993
).
Further research in this area is clearly needed.
Heart rate versus stroke volume regulation during exercise
Increased observed after force
feeding in sea bass was due primarily to tachycardia
(Axelsson et al., 2002
).
Similarly, in the present experiments, sea bass increased
through tachycardia with no
significant change in Vs, despite the fact that cardiac
preload increased significantly (Fig.
3, Table 1). This
shows that an increased cardiac preload does not necessarily lead to an
increased Vs in fish, but may instead compensate for a
reduced cardiac filling time associated with an increase in
fH. Thus, within the scope of the present exercise
challenge,
in sea bass was frequency
regulated.
Other studies on fish with various life-strategies also suggest that
control of by fH
during exercise, might be more important than previously thought
(Farrell, 1991
;
Farrell and Jones, 1992
;
Jones and Randall, 1978
).
Korsmeyer et al. (1997
) found
in the highly active yellowfin tuna (Thunnus albacares) that
increased by 13.6% during exercise at
24°C exclusively through tachycardia and, in fact, Vs
decreased. Similarly, during forced swimming at 0°C the Antarctic borch
(Pagothenia borchgrevinki) increased
by 75% by doubling
fH (Axelsson et al.,
1992
). Furthermore, Cooke et al.
(2003
) investigated the
relative contribution of Vs and fH to
maximum cardiac output at 3°C in three North American species with various
degrees of winter quiescence. Largemouth bass (Micropterus
salmoides), a winter inactive species, increased
by means of a 124% increase in
fH with a 24% reduction in Vs.
Similarly, the intermediately active black crappie (Pomoxis
nigromaculatus) increased
by a
156% increase in fH with a 56% reduction in
Vs. By contrast, in the winter active white bass
(Morone chrysops) maximum
was attained by a 45% increase in fH and a 55% increase in
Vs. Within a species, temperature may modulate the
relative contributions of fH and Vs
during exercise. For example, for maximum
at 5°C and 10°C in largescale
suckers (Catostomus macrocheilus), increased Vs
contributed 58% and 62%, respectively
(Kolok et al., 1993
), whereas
at 16°C fH contributed 70% of maximum
during exercise. Altogether these
results indicate the importance of frequency regulation of
in various fish species under various
conditions but, of course, contrasts with several studies (mainly on
salmonids) where increased Vs was the major means of
increasing
during exercise
(Dunmall and Schreer, 2003
;
Farrell, 1991
;
Farrell and Jones, 1992
;
Jones and Randall, 1978
;
Kiceniuk and Jones, 1977
).
Under the present experimental conditions, exercising sea bass used only
tachycardia to increase , but to what
degree Vs might be modulated in sea bass at higher
swimming speeds and different temperatures awaits further study. By performing
the study at 22°C, which is in the upper range of the temperature
preferendum for sea bass (Claireaux and
Lagardere, 1999
), it is possible that at lower water temperatures
Vs could increase during swimming. Another concern is that
fish only swam to 2 BL s-1 and this resulted in a
relatively small increase in
(38%).
Therefore, it is possible that at higher swimming speeds further increases in
could occur through increased
Vs.
In conclusion, this is the first study to measure variables related to
venous return and cardiac filling pressure during exercise and to provide
evidence for an active involvement of the venous vasculature during exercise
in any species of fish. An -adrenoceptor mediated control system was
partially responsible for a decrease in venous capacitance, as reflected as an
increase in MCFP in the swimming sea bass. This control would serve to: (1)
maintain or increase the pressure gradient for venous return, thus matching
venous return and cardiac output; (2) Increase central venous blood volume,
and consequently cardiac preload; and (3) Possibly redistribute venous blood
to other parts of the circulation, such as the gills and muscle capillaries.
These results highlight the fact that an increased cardiac preload does not
necessarily result in an increased Vs, but can instead
compensate for the reduced filling time when fH is
increased, thereby offsetting potential decreases in Vs.
In fact, under the present conditions, the exercise-induced increase in
in sea bass was exclusively mediated
by tachycardia.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Altimiras, J. and Axelsson, M. (2004).
Intrinsic autoregulation of cardiac output in rainbow trout (Oncorhynchus
mykiss) at different heart rates. J. Exp. Biol.
207,195
-201.
Altimiras, J. and Larsen, E. (2000). Non-invasive recording of heart rate and ventilation rate in rainbow trout during rest and swimming. Fish go wireless. J. Fish. Biol. 57,197 -209.[CrossRef]
Axelsson, M. (1988). The importance of nervous and humoral mechanisms in the control of cardiac performance in the Atlantic cod Gadus morhua at rest and during non-exhaustive exercise. J. Exp. Biol. 137,287 -301.[Abstract]
Axelsson, M., Altimiras, J. and Claireaux, G.
(2002). Post-prandial blood flow to the gastrointestinal tract is
not compromised during hypoxia in the sea bass Dicentrarchus labrax.
J. Exp. Biol. 205,2891
-2896.
Axelsson, M., Davison, B., Forster, M. and Nilsson, S.
(1994). Blood pressure control in the antarctic fish
Pagothenia borchgrevinki. J. Exp. Biol.
190,265
-279.
Axelsson, M., Davison, W., Forster, M. E. and Farrell, A. P. (1992). Cardiovascular responses of the red-blooded antarctic fishes Pagothenia bernacchii and P. borchgrevinki. J. Exp. Biol. 167,179 -201.[Abstract]
Axelsson, M., Driedzic, W. R., Farrell, A. P. and Nilsson, S. (1989). Regulation of cardiac output and gut blood flow in the searaven, Hemitripterus americanus. Fish Physiol. Biochem. 6,315 -326.
Axelsson, M. and Fritsche, R. (1991). Effects of exercise, hypoxia and feeding on the gastrointestinal blood flow in the Atlantic cod Gadus morhua. J. Exp. Biol. 158,181 -198.[Abstract]
Axelsson, M. and Nilsson, S. (1986). Blood pressure control during exercise in the Atlantic cod, Gadus morhua. J. Exp. Biol. 126,225 -236.[Abstract]
Axelsson, M., Thorarensen, H., Nilsson, S. and Farrell, A. P. (2000). Gastrointestinal blood flow in the red Irish lord, Hemilepidotus hemilepidotus: Long-term effects of feeding and adrenergic control. J. Comp. Physiol. 170,145 -152.
Butler, P. J., Axelsson, M., Ehrenstrom, F., Metcalfe, J. D. and Nilsson, S. (1989). Circulating catecholamines and swimming performance in the Atlantic cod Gadus morhua. J. Exp. Biol. 141,377 -388.
Campbell, H. A., Taylor, E. W. and Egginton, S.
(2004). The use of power spectral analysis to determine
cardiorespiratory control in the short-horned sculpin Myoxocephalus
scorpius. J. Exp. Biol.
207,1969
-1976.
Claireaux, G. and Lagardere, J. P. (1999). Influence of temperature, oxygen and salinity on the metabolism of the European sea bass. J. Sea Res. 42,157 -168.[CrossRef]
Conklin, D., Chavas, A., Duff, D., Weaver, L., Zhang, Y. and
Olson, K. R. (1997). Cardiovascular effects of arginine
vasotocin in the rainbow trout Oncorhynchus mykiss. J.
Exp. Biol. 200,2821
-2832.
Cooke, S. J., Grant, E. C., Schreer, J. F., Philipp, D. P. and DeVries, A. L. (2003). Low temperature cardiac response to exhaustive exercise in fish with different levels of winter quiescence. Comp. Biochem. Physiol. A 134,157 -165.
Dunmall, K. M. and Schreer, J. F. (2003). A comparison of the swimming and cardiac performance of farmed and wild Atlantic salmon, Salmo salar, before and after gamete stripping. Aquaculture 220,869 -882.[CrossRef]
Farrell, A. P. (1991). From hagfish to tuna: a perspective on cardiac function in fish. Physiol. Zool. 64,1137 -1164.
Farrell, A. P. and Clutterham, S. M. (2003).
On-line venous oxygen tensions in rainbow trout during graded exercise at two
acclimation temperatures. J. Exp. Biol.
206,487
-496.
Farrell, A. P. and Jones, D. R. (1992). The heart. In Fish Physiology, The Cardiovascular System., vol. XII (ed. W. S. Hoar, D. J., Randall and A. P. Farrell), pp. 1-88. New York: Academic Press Inc.
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. 125,319 -345.[Abstract]
Farrell, A. P., Thorarensen, H., Axelsson, M., Crocker, C. E., Gamperl, A. K. and Cech, J. J., Jr (2001). Gut blood flow in fish during exercise and severe hypercapnia. Comp. Biochem. Physiol. 128A,551 -563.
Forster, M. E. and Farrell, A. P. (1994). The volumes of the chambers of the trout heart. Comp. Biochem. Physiol. A 109,127 -132.[CrossRef]
Franklin, C. E. and Davie, P. S. (1992). Dimensional analysis of the ventricle of an in situ perfused trout heart using echocardiography. J. Exp. Biol. 166, 47-60.[Abstract]
Hoagland, T. M., Weaver, L., Jr, Conlon, J. M., Wang, Y. and Olson, K. R. (2000). Effects of endothelin-1 and homologous trout endothelin on cardiovascular function in rainbow trout. Am. J. Physiol. 278,R460 -R468.
Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65-70.
Jones, D. R. and Randall, D. J. (1978). The respiratory and circulatory systems during exercise. In Fish Physiology (ed. W. S. Hoar and D. J. Randall), pp.425 -492. New York, London: Academic Press.
Kiceniuk, J. W. and Jones, D. R. (1977). The oxygen transport system in trout (Salmo gairdneri) during sustained exercise. J. Exp. Biol. 69,247 -260.
Kolok, A. S., Spooner, R. M. and Farrell, A. P.
(1993). The effect of exercise on the cardiac output and blood
flow distribution of the largescale sucker Catostomus macrocheilus.
J. Exp. Biol. 183,301
-321.
Korsmeyer, K. E., Lai, N. C., Shadwick, R. E. and Graham, J. B. (1997). Heart rate and stroke volume contributions to cardiac output in swimming yellowfin tuna: Response to exercise and temperature. J. Exp. Biol. 20,1975 -1986.
Lefrancois, C., Claireaux, G. and Lagardere, J. P. (1998). Heart rate telemetry to study environmental influences on fish metabolic expenditure. Hydrobiologia 371/372,215 -224.[CrossRef]
Olson, K. R., Conklin, D. J., Farrell, A. P., Keen, J. E., Takei, Y., Weaver, L., Jr, Smith, M. P. and Zhang, Y. (1997). Effects of natriuretic peptides and nitroprusside on venous function in trout. Am. J. Physiol. 273,R527 -R539.[Medline]
Pang, C. C. (2001). Autonomic control of the venous system in health and disease: effects of drugs. Pharmacol. Ther. 90,179 -230.[CrossRef][Medline]
Priede, I. G. (1974). The effect of swimming activity and section of the vagus nerves on heart rate in rainbow trout. J. Exp. Biol. 60,305 -319.[Medline]
Rothe, C. F. (1986). Physiology of venous return. An unappreciated boost to the heart. Arch. Intern. Med. 146,977 -982.[Abstract]
Rothe, C. F. (1993). Mean circulatory filling pressure: its meaning and measurement. J. Appl. Physiol. 74,499 -509.[Abstract]
Sandblom, E. and Axelsson, M. (2005).
Baroreflex mediated control of heart rate and vascular capacitance in trout.
J. Exp. Biol. 208,821
-829.
Smith, D. G. (1978). Neural regulation of blood pressure in rainbow trout (Salmo gairdneri). Can. J. Zool. 56,1678 -1683.
Smith, D. G., Nilsson, S., Wahlqvist, I. and Eriksson, B. M. (1985). Nervous control of the blood pressure in the Atlantic cod, Gadus morhua. J. Exp. Biol. 117,335 -437.[Abstract]
Stevens, E. D. and Randall, D. J. (1967). Changes in blood pressure, heart rate and breathing rate during moderate swimming activity in rainbow trout. J. Exp. Biol. 46,307 -315.[Medline]
Thorarensen, H., Gallaugher, P. E., Kiessling, A. K. and
Farrell, A. P. (1993). Intestinal blood flow in swimming
chinook salmon Oncorhynchus tshawytscha and the effects of
haematocrit on blood flow distribution. J. Exp. Biol.
179,115
-129.
Zhang, Y., Weaver, L., Jr, Ibeawuchi, A. and Olson, K. R. (1998). Catecholaminergic regulation of venous function in the rainbow trout. Am. J. Physiol. 274,R1195 -R1202.[Medline]