|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online August 17, 2007
Journal of Experimental Biology 210, 3068-3074 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.003137
Antarctic fish can compensate for rising temperatures: thermal acclimation of cardiac performance in Pagothenia borchgrevinki
1 School of Integrative Biology, The University of Queensland, Brisbane, QLD
4072, Australia
2 School of Biological Sciences, The University of Canterbury, Christchurch,
New Zealand
3 School of Biological Sciences, The University of Sydney, Sydney, NSW 2001,
Australia
* Author for correspondence (e-mail: c.franklin{at}uq.edu.au)
Accepted 27 June 2007
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: fish, Antarctica, cardiac output, heart, specialist, acclimation, thermal plasticity, chronotropic
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
), and
particularly on thermal specialists (stenotherms) that lack the ability to
physiologically compensate for a rise in water temperature. Ectothermic
organisms found in the cold and stable waters of the Southern Ocean close to
the Antarctic continent are often regarded as the archetypal thermal
specialists. They experience body temperatures close to the freezing point of
seawater (–1.9°C), and annual temperature fluctuations are less than
1°C (Clarke and Johnston,
1996; Hunt et al.,
2003). The finding that small acute increases in water temperature
dramatically reduced the maximum sustainable swimming performance
(Ucrit) of a cryopelagic Antarctic fish, Pagothenia
borchgrevinki (Wilson et al.,
2002) lends support for the concerns raised about the impact of
global warming. The respiratory factorial scope (the difference between
ventilation rates at rest and at Ucrit) in these fish
decreased with increasing temperatures, such that at 6°C there was no
difference between resting and maximal ventilation rates and, hence, no scope
for the increased oxygen requirements during exercise
(Wilson et al., 2002).
Aerobic swimming performance of fish is closely associated with the
functioning of the cardiovascular system and the ability of the heart to
provide an adequate supply of oxygen and metabolites to the working muscles.
During swimming, fish augment cardiac output by a combination of increases in
heart rate and stroke volume, thereby increasing oxygen delivery to the
tissues (Axelsson, 1988;
Farrell, 1991;
Shiels et al., 2002). The
relative contributions of stroke volume and heart rate to increases in cardiac
output vary among species. Some fish increase cardiac output predominantly by
an elevation in heart rate (e.g. tuna), while others mainly employ increases
in stroke volume [e.g. rainbow trout
(Farrell, 1991;
Franklin and Davie,
1992)].
Cardiac function in fish is also profoundly influenced by changes in
temperature (Taylor et al.,
1996; Farrell et al.,
1996; Farrell,
2002). An acute rise in water temperature increases resting
cardiac output in fish, chiefly as a result of increased heart rate
(Gollock et al., 2006).
Increases in heart rate and cardiac output with acute increases in temperature
may be the consequence of the direct thermal effects on the intrinsic rate of
physiological processes. Additionally, heart rate may increase to compensate
for the reduction in oxygen carrying capacity at higher temperatures, thereby
ensuring constant oxygen delivery to the tissues
(Taylor et al., 1996;
Taylor et al., 1997). In fish,
cardiac scope decreases with an acute increase in water temperature, resulting
in a decrease in Ucrit
(Farrell, 1997). Generally,
acute increases in temperature elevate both resting and maximal cardiac
output. However, if the thermal dependence of resting cardiac output is
greater than that of maximal cardiac output, cardiac scope will be reduced at
higher temperatures (Farrell,
2002).
Phenotypic flexibility in response to thermal fluctuation [acclimatisation,
acclimation (Piersma and Drent,
2003)] provides a physiological strategy that allows animals to
compensate for environmental temperature change
(Wilson and Franklin, 2002).
Acclimation or acclimatisation allows ectotherms to maintain physiological
function and performance across a wide thermal range, and it is often
associated with species that experience pronounced seasonal changes in
temperature (Huey and Hertz,
1984; Guderley and St-Pierre,
2002). As such, phenotypic flexibility is not predicted to be an
attribute characteristic of stenothermal fish
(Somero and DeVries, 1967)
living in the cold and highly stable waters of the Southern Ocean, and indeed
it is currently believed that there has been a trade-off between thermal
tolerance and the ability to live in extreme cold waters
(Pörtner et al., 2000).
Hence, it was surprising that P. borchgrevinki was found to thermally
acclimate sustained swimming performance
(Seebacher et al., 2005).
P. borchgrevinki exposed to 4°C for 4–5 weeks compensated
their aerobic swimming performance such that after acclimation,
Ucrit at 6°C was not significantly different from that
at –1°C in cold (–1°C) acclimated fish. The ability to
maintain their swimming performance (i.e. Ucrit) at
6°C would be expected to be accompanied by changes in their cardiovascular
system that allowed for a maintenance of factorial scope for cardiac output.
Therefore, the aim of this study was to assess the mechanisms allowing warm
acclimated P. borchgrevinki to maintain factorial scope for cardiac
output, and hence aerobic scope and Ucrit, at higher
temperatures.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Surgery
Fish were anaesthetised in MS222 (1:5000) and transferred to a surgical
sling. To maintain anaesthesia during surgery, the gills were irrigated with
seawater containing 1:10 000 MS222. The ventral aorta was exposed via
a small mid-ventral incision and a single-crystal Doppler flow probe placed
around the vessel, just distal to the pericardium. The Doppler crystals were
incorporated into cuffs (1–2 mm diameter) that were custom made from
PerspexTM. The PerspexTM provided a more secure fit around ventral
aorta than the silicone cuffs provided by Iowa Doppler Products. The incision
was closed with silk sutures (Ethicon 4-0) and the leads from the Doppler flow
probe secured to the body wall. This procedure took approximately 10 min to
complete. Fish were returned to tanks at their acclimation temperatures and
allowed to recover for 24 h before recording and experimentation.
Experimental setup
For each acclimation group, the cardiac performance of eight fish was
examined (body mass: –1°C, 88.9±15.1 g; 4°C,
91.1±11.8 g; means ± s.d.). Individual fish were transferred to
an experimental tank (70 cmx40 cmx20 cm lengthxwidthx
height) and the leads from the flow probe connected to a Doppler flowmeter
(Iowa University, Iowa City, IA, USA, Model 545C-4). Signals from the
flowmeter were directed to a computerised recording system (Powerlab,
ADInstruments, Sidney, NSW, Australia) sampling at 40 Hz and displayed on a
Toshiba laptop computer running Chart software (ADInstruments). Heart rate
(fH) was determined from the pulsatile flow signals using
Chart.
Calibration of the Doppler flow probes was undertaken in situ at
the completion of the experimental treatments. Fish were euthanased with an
overdose of MS222 and a blood sample (approx. 1 ml) taken from the caudal
vessels with a heparinised syringe (21-gauge needle). The heart was exposed
and a polyethylene cannula inserted into the bulbous arteriosus and tied
firmly in place. A peristaltic pump (Gilson Minipuls, Villers-le-Bel, France),
passed blood diluted with saline (to a haematocrit of approx. 8%) through the
cannula and ventral aorta at known flow rates (for details, see
Axelsson et al., 1992).
Experimental protocol
Fish with implanted flow probes were transferred from the acclimation tanks
to the experimental tank at their acclimation temperature (–1°C or
4°C) and left undisturbed for 4 h. Previous work had shown that this was
sufficient time for cardiovascular parameters to return to resting levels
(Lowe et al., 2005). Cardiac
output (
) was continuously recorded at
rest and after exhaustive exercise, which was achieved by chasing and tapping
the tail of the fish with a spatula for 5 min. Measurements were taken at
rest, and for 30 min after exhaustive exercise. Measurements were not taken
during the forced exercise period as the signal from the flow probe was
erratic. Fish were transferred from their holding tanks into the experimental
chamber and initially tested at their acclimation temperature. They were then
randomly tested at –1, 2, 4, 6 and 8°C, allowing 6 h recovery (at
their acclimation temperature) between test temperatures. Temperature was
increased or decreased in the experimental chamber at a rate of 2°C
h–1.
Analysis
Measurements of cardiac function (cardiac output and heart rate) were made
during rest, exercise and recovery. Cardiac function was measured every
4–5 min, taking mean values for blocks of 30–60 s. Shorter
sampling periods (30 s) were required immediately after exercise as cardiac
function changed rapidly during this period. Stroke volume
(VS) was calculated from
/fH. Factorial
scope for cardiac output, heart rate and stroke volume was calculated by
dividing maximal values (immediately after exercise) by resting values.
The effect of exercise and recovery time on
, VS and
fH were analysed by a one-way repeated-measures ANOVA. The
effect of exercise and test temperature on
, VS and
fH were analysed with a two-way repeated-measures ANOVA.
The effect of acclimation temperature and test temperature on
, VS and
fH were analysed with a two-way repeated-measures ANOVA.
Pairwise comparisons were analysed using t-tests. Results were
considered significant at P<0.05. All results are presented as
means ± s.e.m.
|
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
In P. borchgrevinki acclimated to –1°C, there was a significant increase in resting cardiac output with increasing temperature (Fig. 2A; F7,4=10.50, P<0.001; Q10[–1°C to 8°C]= 1.62). At –1°C, resting cardiac output of –1°C acclimated P. borchgrevinki was 22.2±2.9 ml min–1 kg–1 body mass and, upon exposure to 8°C, resting cardiac output increased by 54% to 34.2±2.9 ml min–1 kg–1 body mass. In contrast to the –1°C acclimated P. borchgrevinki, the exposure of the 4°C acclimated fish to an acute temperature change, resulted in higher resting cardiac outputs at lower temperatures (Fig. 2B; F7,4=5.26, P<0.01). After acclimation to 4°C, resting cardiac output at 4°C was not significantly different from resting cardiac output of the –1°C acclimated fish at –1°C, demonstrating compensation of resting cardiac output with acclimation at higher temperatures. An acute change in temperature had no significant effect upon maximal cardiac output across the test temperatures in either the –1°C or 4°C acclimated P. borchgrevinki (Fig. 2A,B). Maximal cardiac outputs of the –1°C and 4°C acclimated fish at –1°C and 4°C, respectively, were also not significantly different.
|
|
There was a significant effect of exercise on heart rate across test temperatures in the 4°C acclimated fish (F1,4=5.58, P<0.01). Resting heart rates of the 4°C acclimated P. borchgrevinki were thermally independent between –1°C and 8°C (Fig. 3B). However, maximal heart rates were significantly affected by temperature (Fig. 3B; F7,4=66.9, P<0.001). At –1°C, heart rate reached a maximum of 29.1±0.7 beats min–1 with exercise, whereas at 8°C, the maximum recorded heart rate was 46.2±2.0 beats min–1 (Q10[–1°C to 8°C]=1.68). Therefore in the 4°C acclimated fish, as temperature increased, so did scope for heart rate (Fig. 3B). Resting heart rates of the –1°C and 4°C acclimated fish at –1°C and 4°C, respectively (–1°C 19.0±0.9 beats min–1; 4°C 20.8±3.2 beats min–1) were not significantly different from each other; however, the maximal heart rate of the 4°C acclimated fish at 4°C (41.5± 1.3 beats min–1) was significantly higher (P<0.001) than the maximal heart rate of the –1°C acclimated fish at –1°C (27.6±0.7 beats min–1).
There was a significant increase in stroke volume with exercise across test temperatures in the –1°C acclimated P. borchgrevinki (Fig. 4A; F1,4=4.99, P<0.01). There was no effect of temperature on stroke volume of –1°C acclimated fish at rest; however, with exercise there was a significant decrease in stroke volume with increasing temperature (Fig. 4A; F7,4=4.69, P<0.01). Stroke volume during exercise decreased from 2.14±0.34 ml kg–1 at –1°C, to 1.25±0.20 ml kg–1 at 8°C. In the 4°C acclimated P. borchgrevinki, exercise had no effect on stroke volume across test temperatures (Fig. 4B; F1,4=0.361, P=0.83). Acute increases in water temperature between –1°C and 8°C resulted in a small decrease in stroke volume at rest and during/after exercise in the 4°C acclimated fish (Fig. 4B).
|
At an ambient temperature of –1°C, P. borchgrevinki acclimated to –1°C had a significantly greater cardiac scope than fish acclimated to 4°C (P<0.01). In the –1°C acclimated fish at –1°C, cardiac output increased with exercise from 22.2±2.92 to 59.5±10.1 ml min–1 kg–1 body mass, representing a factorial cardiac scope of 2.62 (Fig. 2A and Fig. 5A). In contrast, the cardiac output of 4°C acclimated P. borchgrevinki exercised at –1°C had a factorial scope of 1.43, with cardiac output only increasing from 30.6±3.1 to 43.8±4.4 ml min–1 kg–1 (Fig. 2B and Fig. 5A).
|
In the –1°C acclimated fish, the increase in cardiac output with exercise at –1°C was due to increases in both heart rate and stroke volume (Fig. 3A, Fig. 4A, Fig. 5B,C). With exercise at –1°C, heart rate increased from 19.1±0.9 to 27.6± 0.7 beats min–1 (factorial scope for heart rate=1.50±0.08) and stroke volume increased from 1.20±0.16 to 2.14± 0.34 ml kg–1 body mass (factorial scope for stroke volume= 1.76±0.13) (Fig. 3A, Fig. 4A). The decrease in factorial scope for cardiac output of the –1°C acclimated fish at the higher ambient temperatures could be attributed to a significant decrease in factorial scope for heart rate combined with a drop in factorial scope for stroke volume (Fig. 5A–C).
There was a significant difference in the factorial scope for heart rate between the –1 and 4°C acclimated fish across the test temperatures (F1,4=13.35, P<0.001) but not in factorial scope for stroke volume (F1,4=1.72, P=0.159). The maintenance of factorial scope for cardiac output in the 4°C acclimated fish between 2–8°C was due to changes in heart rate alone (Fig. 5A–C). Stroke volume did not change with exercise and hence did not contribute to scope for cardiac output in 4°C acclimated P. borchgrevinki (Fig. 4B, Fig. 5C). At –1°C, the decrease in factorial scope for cardiac output of the 4°C acclimated fish could be attributed to a decrease in factorial scope for heart rate (Fig. 5A,B).
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
), but is in contrast to another, which found that heart rate
was thermally independent between –1 and 3°C
(Franklin et al., 2001). The
different thermal responses of the cardiovascular system of P.
borchgrevinki are possibly due to the rate and magnitude of the
temperature increases, with the temperature increase in the present study and
in Lowe et al. (Lowe et al.,
2005) being considerably larger and more rapid than that of
Franklin et al. (Franklin et al.,
2001). In the present study, subjecting the –1°C
acclimated fish to acute increases in temperature up to 8°C had a positive
chronotropic effect on the heart at both rest and with exercise. Stroke
volume, however, remained unaffected at rest by an increase in temperature,
and with exercise there was a negative influence on stroke volume, with a
marked reduction being observed at high temperatures. In general, acute
increases in temperature have a positive chronotropic and negative intropic
effect on the myocardium of fish, resulting in a reduction of maximum cardiac
power output (Farrell et al.,
1996; Gamperl and Farrell,
2004). While there was no significant decrease in maximum cardiac
output at high temperatures, factorial scope for cardiac output was severely
compromised. In the –1°C acclimated fish, the factorial scope for
cardiac output was greatest at –1°C with increase in cardiac output
at –1°C after exercise being the result of near equal increases in
both heart rate and stroke volume. When exposed to water temperatures of
4–8°C there was a marked reduction in scope for cardiac output, and
at 8°C maximal cardiac output was only 10% higher than resting cardiac
output. At the higher temperatures, there was virtually no scope for heart
rate, with maximal heart rates with exercise being close to resting heart
rates. Only stroke volume contributed significantly to the increase in cardiac
output at the high temperatures. The observed detrimental affects of an
increase in temperature on scope for cardiac output in P.
borchgrevinki would contribute to the reduction in sustained swimming
performance of this fish at higher temperatures, and its narrow thermal
swimming performance breadth (Wilson et
al., 2002). The reduction in swimming performance would also
result from a decrease in O2 binding affinity and O2
carrying capacity at higher temperatures as a consequence of a right shift of
the oxygen equilibrium curve (Farrell,
2002; Taylor et al.,
1996; Taylor et al.,
1997).
Farrell suggested that cardiac oxygen supply in fish may become limited at
high temperatures due to lowered venous oxygen levels
(Farrell, 2002). The lower
oxygen levels would become insufficient to meet cardiac oxygen demand,
resulting in a reduction in the ability of the myocardium to maintain cardiac
scope. While this may be a factor in compromising cardiac function in P.
borchgrevinki at high acute temperatures, maximum cardiac output was
maintained from –1°C to 8°C in –1°C acclimated fish,
and rather it was the inability of P. borchgrevinki to regulate
resting cardiac output via heart rate that resulted in a reduction in
cardiac scope. The increase in cardiac output with an increase in temperature
under resting conditions is most likely due to the thermal dependence of
metabolism and the requirement to increase oxygen delivery to the tissues at
higher temperatures (Wilson et al.,
2002).
When exposed to elevated temperatures (4°C) for a prolonged period
P. borchgrevinki fully compensated for the negative effects of high
temperatures, and sustained swimming performance was restored
(Seebacher et al., 2005). With
acclimation to 4°C, scope for cardiac output was maintained at 4, 6 and
8°C, resulting in the thermal compensation of cardiac function at the
higher temperatures. This however, was at the expense of cardiac performance
at –1°C, where there was a significant decrease in cardiac scope.
This reduction in scope for cardiac output of the 4°C acclimated fish at
–1°C was attributed to a lack of scope for stroke volume; that is,
stroke volume did not change with exercise.
While increases in cardiac output with exercise in the –1°C acclimated fish at 1°C were achieved by increases in both heart rate and stroke volume, increases in cardiac output with exercise in the 4°C acclimated fish were achieved by changes in heart rate alone, with stroke volume not varying between rest and exercise at any test temperatures. This striking difference between thermal acclimation groups represents a change in pumping strategy from a mixed inotropic/chronotropic modulated heart in –1°C acclimated P. borchgrevinki to a purely chronotropic modulated heart in the 4°C acclimated fish.
Cardiac plasticity in response to thermal acclimation has been reported for
a number of fish species (Gamperl and
Farrell, 2004), although the marked change in pumping strategy
seen in P. borchgrevinki to chronic temperature exposure has not been
noted previously. Thermal compensation of maximum cardiac output and maximum
power output occurs in rainbow trout with Q10 values of
1.2–1.4 between 5°C and 18°C
(Graham and Farrell, 1989;
Keen and Farrell, 1994).
Q10 values for factorial scope of cardiac output in P.
borchgrevinki are also reduced with acclimation, having equivalent scopes
when tested at their acclimation temperatures, indicating thermal
compensation. Increases in ventricular muscle mass occur with cold acclimation
in rainbow trout, which offsets the decrease in contractility at lower
temperatures, thereby maintaining stroke volume
(Gamperl and Farrell, 2004).
The intrinsic cardiac pacemaker rate is reset with cold acclimation in rainbow
trout and involves changes to membrane ion channel function and density
(Vornanen et al., 2002). This
mechanism warrants investigation in P. borchgrevinki, given the
change in pumping strategy to a chronotropic driven heart with acclimation to
4°C.
The maintenance of cardiac function in P. borchgrevinki with
acclimation to 4°C could result from thermal compensation of metabolism at
the higher temperature and a corresponding reduction in oxygen demand. This is
likely, as resting cardiac output was reduced at 4°C acclimated fish
compared with –1°C acclimated fish. The stenothermal gadoid,
Lota lota, can survive high summer water temperatures because it is
able to downregulate its aerobic metabolism
(Hardewig et al., 2004).
Surprisingly, the thermal acclimation of resting metabolic rate has not been
studied in P. borchgrevinki, although metabolic capacities (i.e.
lactate dehydrogenase and cytochrome c oxidase activities) increased
with warm acclimation (Seebacher et al.,
2005).
In Antarctic fish, the cholinergic system strongly regulates heart rate and
the cholinergic tone increased with an acute increase in temperature
(Axelsson et al., 1992;
Axelsson et al., 1994;
Franklin et al., 2001;
Lowe et al., 2005). Thermal
acclimation has been shown to alter the extrinsic modulation of the heart
affecting the relative contributions from the cholinergic and adrenergic
systems. Wood et al. found that cholinergic tone increased with cold
acclimation in rainbow trout, and that adrenergic tone was more important at
higher temperatures (Wood et al.,
1979). Again, this aspect of cardiac control with thermal
acclimation warrants further investigation in P. borchgrevinki.
The thermal sensitivity of factorial scope for cardiac output provides an
excellent indicator of cardiac performance in response to temperature
(Farrell, 2002). The greatest
impact of a change in temperature can be seen on scope for cardiac output in
P. borchgrevinki. An acute increase in temperature negatively
affected scope for cardiac output in the –1°C acclimated fish, and
conversely a decrease in temperature had a deleterious effect on scope in the
4°C acclimated fish. Investigating only the acute effects of temperature
on resting and/or maximal cardiac performance would have failed to detect
significant negative effects on cardiac performance unless at extreme
temperatures, where cardiac function would be severely compromised and
arrhythmias often result (Farrell,
2002; Gollock et al.,
2006).
The compensation of cardiac and swimming performance
(Seebacher et al., 2005) in
P. borchgrevinki with thermal acclimation is contrary to the general
dogma that Antarctic fish are stenothermal and highly specialised to the very
stable and cold waters of the Antarctic
(Somero et al., 1996).
Evolutionary theory predicts that specialisation to a narrow set of
environmental conditions will result in a decrease in capacity for an
organism's phenotype to change in response to environmental change and
variability (Huey and Hertz,
1984). Antarctic fish from high latitudes are often regarded as
the archetypal thermal specialists (Somero
and DeVries, 1967; Wilson et
al., 2002; Johnston,
2003). However, the ability of P. borchgrevinki to
thermally acclimate and in so doing increase performance breadth over a range
of temperatures not experienced on an annual basis, calls for a re-evaluation
of the basis of thermal specialisation in Antarctic fish. This is perhaps not
surprising given that P. borchgrevinki evolved from an ancestral
stock of temperate fishes (Eastman,
1993), and that despite the present cold and stable temperatures
of the Southern Ocean, fishes from the Antarctic waters have been exposed to
episodic periods of warming and cooling over geological time
(Clarke and Johnston, 1996).
This temperature variation provides the necessary driver for thermal
plasticity.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Axelsson, M. (1988). The importance of nervous
and humoral mechanisms in the control of cardiac performance in Atlantic cod,
at rest and during exercise. J. Exp. Biol.
137,287
-303.
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.
Axelsson, M., Davison, W., Forster, M. E. and Nilsson, S. (1994). Blood pressure control in the Antarctic fish Pagothenia borchgrevinki. J. Exp. Biol. 190,265 -279.[Abstract]
Clarke, A. and Johnston, I. A. (1996). Evolution and adaptive radiation of Antarctic fishes. Trends Ecol. Evol. 11,212 -218.[CrossRef]
Eastman, J. T. (1993). Antarctic Fish Biology: Evolution in a Unique Environment. San Diego: Academic Press.
Farrell, A. P. (1991). From hagfish to tuna – a perspective on cardiac function. Physiol. Zool. 64,1137 -1164.
Farrell, A. P. (1997). Effects of temperature on cardiovascular performance. In Global Warming: Implications for Freshwater and Marine Fish (Society for Experimental Biology Seminar Series 61) (ed. C. M. Wood and D. G. McDonald), pp.135 -158. Cambridge: Cambridge University Press.
Farrell, A. P. (2002). Cardiorespiratory performance in salmonids during exercise at high temperature: insights into cardiovascular design limitations in fishes. Comp. Biochem. Physiol. 132,797 -810.
Farrell, A. P., Gamperl, A. K., Hicks, J. M. T., Shiels, H. A. and Jain, K. E. (1996). Maximum cardiac performance of rainbow trout (Oncorhynchus mykiss) at temperatures approaching their upper lethal limit. J. Exp. Biol. 199,663 -672.[Abstract]
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.
Franklin, C. E., Axelsson, M. and Davison, W. (2001). Constancy and control of heart rate during an increase in temperature in the Antarctic fish Pagothenia borchgrevinki. Exp. Biol. Online 6,1 -8.[CrossRef]
Gamperl, A. K. and Farrell, A. P. (2004).
Cardiac plasticity in fishes: environmental influences and intraspecific
differences. J. Exp. Biol.
207,2539
-2550.
Gollock, M. J., Currie, S., Petersen, L. H. and Gamperl, A.
K. (2006). Cardiovascular and haematological responses of
Atlantic cod (Gadus morhua) to acute temperature increase.
J. Exp. Biol. 209,2961
-2970.
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.
Guderley, H. and St-Pierre, J. (2002). Going
with the flow or life in the fast lane: contrasting mitochondrial responses to
thermal change. J. Exp. Biol.
205,2237
-2249.
Hardewig, I., Portner, O. and van Dijk, P. (2004). How does the cold stenothermal gadoid Lota lota survive high water temperatures during summer? J. Comp. Physiol. B 174,149 -156.[CrossRef][Medline]
Huey, R. B. and Hertz, P. E. (1984). Is a jack-of-all temperatures a master of none? Evolution 38,441 -444.[CrossRef]
Hunt, B., Hoefling, K. and Cheng, C. H. C. (2003). Annual warming episodes in seawater temperatures in McMurdo Sound in relationship to endogenous ice in notothenioid fish. Antarct. Sci. 15,333 -338.[CrossRef]
Johnston, I. A. (2003). Muscle metabolism and growth in Antarctic fishes (suborder Nototheniodei): evolution in a cold environment. Comp. Biochem. Physiol. 136B,701 -713.[CrossRef][Medline]
Keen, J. E. and Farrell, A. P. (1994). Maximum prolonged swimming speed and maximum cardiac performance of rainbow trout, Oncorhynchus mykiss, acclimated to two different water temperatures. Comp. Biochem. Physiol. 108A,287 -295.
Lowe, C. J., Seebacher, F. and Davison, W. (2005). Thermal sensitivity of heart rate and insensitivity of blood pressure in the Antarctic notothenlid fish Pagothenia borckgrevinki.J. Comp. Physiol. B 175,97 -105.[CrossRef][Medline]
Piersma, T. and Drent, J. (2003). Phenotypic flexibility and the evolution of organismal design. Trends Ecol. Evol. 18,228 -233.[CrossRef]
Pörtner, H. O., Van Dijk, P. L. M., Hardewig, I. and Sommer, A. (2000). Levels of metabolic cold adaptation: tradeoffs in eurythermal and stenothermal ectotherms. In Antarctic Ecosystems: Models for Wider Ecological Understanding (ed. W. Davison, C. Howard-Williams and P. Broady), pp.109 -122. Christchurch: New Zealand Natural Sciences.
Seebacher, F., Davison, W., Lowe, C. J. and Franklin, C. E. (2005). Falisfying the thermal specialization paradigm: elevated temperatures do not compromise Antarctic fish. Biol. Lett. 1,151 -154.[CrossRef][Medline]
Shiels, H. A., Vornamen, M. and Farrell, A. P. (2002). The force-frequency relationship in fish hearts – a review. Comp. Biochem. Physiol. 132A,811 -826.[CrossRef][Medline]
Somero, G. N. and DeVries, A. L. (1967).
Temperature tolerance of some Antarctic fishes.
Science 156,257
-258.
Somero, G. N., Dahlhoff, E. and Lin, J. J. (1996). Stenotherm and eurytherms: mechanisms establishing thermal optima and tolerance ranges. In Animals and Temperature: Phenotypic and Evolutionary Adaptation (Society of Experimental Biology Seminar Series 59) (ed. I. A. Johnston and A. F. Bennett), pp.53 -77. Cambridge: Cambridge University Press.
Taylor, E. W., Egginton, S., Taylor, S. E. and Butler, P. J. (1997). Factors which may limit swimming performance at different temperatures. In Global Warming: Implications for Freshwater and Marine Fish (Society for Experimental Biology Seminar Series 61) (ed. C. M. Wood and D. G. McDonald), pp. 105-134. Cambridge: Cambridge University Press.
Taylor, S. E., Egginton, S. and Taylor, E. W. (1996). Respiratory and morphometric limits to maximal sustainable exercise in the rainbow trout with seasonal temperature acclimatization. J. Exp. Biol. 199,835 -845.[Abstract]
Vornanen, M., Shiels, H. A. and Farrell, A. P. (2002). Plasticity of excitation-contraction in fish cardiac myocytes. Comp. Biochem. Physiol. 132A,827 -846.
Wilson, R. S. and Franklin, C. E. (2002). Testing the beneficial acclimation hypothesis. Trends Ecol. Evol. 17,66 -70.[CrossRef]
Wilson, R. S., Kuchel, L. J., Franklin, C. E. and Davison, W. (2002). Turning up the heat on subzero fish: thermal dependence of sustained swimming in an Antarctic notothenioid. J. Therm. Biol. 27,381 -386.[CrossRef]
Wood, C. M. and McDonald, D. G. (1996). Global Warming: Implications for Freshwater and Marine Fish. Society for Experimental Biology Seminar Series 61. Cambridge: Cambridge University Press.
Wood, C. M., Pieprzak, P. and Trott, J. N. (1979). The influence of temperature and anaemia on the adrenergic and cholinergic mechanisms controlling heart rate in the rainbow trout. Can. J. Zool. 57,2440 -2447.
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
significant difference in
cardiac output from resting levels (time=0 min) for 4°C acclimated
fish.
