Temperature is a powerful environmental factor,
which has prominent effects growth, nutrition, reproduction, distribution and
behaviour of fishes (Brett, 1971). Temperature determines the rate of
biochemical reactions and metabolism and thereby sets demands on blood
circulation and cardiac function. Therefore, it is understandable that
temperature has a strong effect on cardiac function.


1.6.1  Significance of heart rate (fH)
in thermal responses of fish heart


The volume of blood circulated through the
heart in one minute is called cardiac output. It is the product of fH
and stroke volume. In exercising fish, changes in cardiac output are achieved
by increases in both SV and fH, while fH is
the main factor in regultation of cardiac output during acute temperature
changes (Randall, 1982; Gollock et al., 2006; Steinhausen et al., 2008;
Mendonça and Gamperl, 2010; Farrell and Smith, 2017) (Brett, 1971; Cech et al.,
1976; Pörtner, 2001; Vornanen et al., 2002; Gamperl and Farrell, 2004; Gollock
et al., 2006; Steinhausen et al., 2008; Mendonça and Gamperl, 2010; Badr et al., 2016). This
is why fH is considered as one of the key physiological variables in
environmental adaptation and acclimation of aquatic vertebrates.

Rate and rhythm
of fish heart originate from the sinoatrial pacemaker. Increase of temperature
increases the discharge rate of pacemaker APs by an unknown mechanism: fH
varies from a few heartbeats per minute (bpm) at near zero temperatures of the
cold-adpated teleosts to the maximum of about 300 bpm in the tropical fish
species (Lillywhite et al., 1999; Gollock et al., 2006; Mendonça and Gamperl,
2010) (Rantin et al., 1998; Lin et al., 2014; Sidhu et al., 2014;
Vornanen and Hassinen, 2016).

Chronic changes
in water temperature induce compensatory changes in fH (Vornanen,
2016). In seasonally acclimatized plaice (Pleuronectes platessa) and
thermally acclimated rainbow trout, physiological adjustment to low
temperatures induces increrases in fH by shortening the
duration of pacemaker AP and without any changes in the steepness of diastolic
depolarization (Harper et al., 1995; Haverinen and Vornanen, 2007). In contrast,
fH in the cold acclimated Pacu (Piaractus mesopotamicus),
goldfish (Carassius auratus) and crucian carp (Carassius carassius) is higher than that in warm acclimated species
mates (Morita and Tsukuda, 1995; Aguair et.al., 2002; Matikainen and Vornanen).
These are examples of the so called reverse or inverse thermal compensation,
and probably associted with the dormant life style of these species in the cold
season. Evidently, temperature-induced changes in fH not
uniform among teleosts, and can be dependent on the species-specific adaptation
“strategy” of the fish to its habitat. Positive thermal compensation improves
cardiac output in the cold by opposing the direct depressive effect of
temperature on fH. Inverse thermal compensation may reduce cardiac
output in the cold, but it also reduces energy consumption of the heart and
thereby is a part of the whole body metabolic depression.

physiological signficance of fH in thermal responses of fish heart
appears in the temperature-induced cardiac arrhythmias. Acute temperature
changes cause different types of arrhythmias in fish hearts, which appear when
temperature approaches or exceeds upper crtitical temperature of the fish.
Cardiac arrhythmias reported in fish hearts include missed beats, bradycardia,
and bursts of rapid beating, and complete cessation of heartbeat (asystole) (Casselman
et al., 2012; Anttila et al., 2013; Verhille et al., 2013; Ferreira et al.,
2014; Vornanen et al., 2014; Badr
et al., 2016).


1.6.2  Effect of temperature on cardiac action


Acute temperature changes significantly change
the shape of pacemaker, atrial and ventricular APs of fish hearts by altering
the flow of inward and outward currents through SL ion channels (Harper et al.,
1995; Vornanen et al., 2002; Haverinen and Vornanen, 2007; Haverinen and
Vornanen, 2009; Ballesta et al., 2012; Vornanen et al., 2014; Lin et al., 2014;
Hassinen et al., 2014; Shiels et al., 2015). Duration of AP must inversly
correlate with fH to allow sufficient time for systole and
diastole; under high fH AP must shorten to allow enough time
for diastolic filling of the heart with blood (Shiels et al., 2002). Therefore,
exercising fish, active fish species like tunas and tropical fishes (e.g.
zebrafishes) living at high temperatures have higher fH and
shorter duration of AP in comparison to cold dormant fishes like crucian carp
or fishes that live in the cold polar waters (antactic fishes) (viitteet).

The shape and
duration of cardiac AP, and the underlying ion currents, are highly sensitive
to chronic temperature changes and crucial in acclimation or acclimatization of
both freshwater and marine teleosts to seasonal temperature regimes. In many
fish species acclimation to cold induces a compensatory decrease in AP
duration, e.g. ….. (Haverinen and Vornanen, 2009; Galli et al., 2009; Hassinen
et al., 2014; Abramochkin and Vornanen, 2015; Vornanen and Hassinen, 2016). This
makes room for the cold-induced increase in fH.


1.6.3  Effects of temperature on ionic currents and channels


Cardiac ion currents and shape of cardiac
AP are affected by acute and chronic temperature changes. The diffusion of ion
through the pore of ion channel is weakly temperature-dependent (Q10 about
1.3), while opening and closing of ion channels are more strongly dependent on
temperature (Q10>2.0). Acute increases in temperature increase density and
kinetics of ion currents up to the TBP, where function of the
channels starts to deteriorate. The inward rectifier K+ channels
(Kir2) are “gated” by voltage-dependent blocking and unblocking of the channel
pore by intracellular Mg2+ and polyamines, and therefore IK1
is only weakly dependent on temperature. In contrast, the genuinly
voltage-gated Na+, K+ and Ca2+ ion channels
are more strongly temperature-dependent, similar as the catalytic activity of
enzymes. (Shiels et al., 2000; Shiels et al., 2006; Galli et al., 2011; Shiels
and Galli, 2014; Vornanen et al., 2014; Kubly and Stecyk, 2015). (Paajanen and
Vornanen, 2004; Haverinen and Vornanen, 2009; Galli et al., 2009; Abramochkin
and Vornanen, 2015).

Thermal acclimation
or acclimatization also affect the density of ion currents and AP shape
(Haverinen and Vornanen, 2009). Inward rectifier K+ current (IK1),
delayed rectifier K+ current (IKr) and Na+
current (INa) are all modified by thermal acclimation (viitteet). The
most consistent response to thermal acclimation is noticed for IKr.
In most fishes, IKr is upregulated by cold-acclimation, i.e. the
density of IKr is higher in cold acclimated fishes than in warm
acclimated fishes (Haverinen and Vornanen, 2009; Galli et al., 2009; Hassinen
et al., 2014; Abramochkin and Vornanen, 2015). Moreover, there is a close
correlation between the density of IKr and fH in
cold- and warm-acclimated fishes (Vornanen, 2016), indicating the importance of
this current in adjusting AP duration to fH.

response of IK1 is species- and chamber-specific. In some fishes it
is increased by cold-acclimation (…), in others it is depressed by
cold-acclimation (e.g. ….) and in still others (e.g.….) there is no response to
chronic temperature changes. Also, there are sometimes differences in thermal
response between atrial and ventricular IK1 in the same fish. For
example, the density of IK1 is higher in atrial myocytes of warm-acclimated
burbot and Pacific bluefin tuna (Thunnus thynnus) than in the cold-acclimated
species mates, while the opposite is true for ventricular myocytes (Haverinen
and Vornanen, 2009; Galli et al.,  2009).
Since IK1 regulates RMP, increase and decrease in the density of IK1
will reduce and enhance excitability, respectively.

The response of
INa to thermal acclimation is also species-specific. INa
is up-regulated in the cold-active rainbow trout and down-regulated in the cold-dormant
crucian carp. Increase and decrease in INa density enhances and
depresses cardiac excitability, respectively. Thus, the species-specific
responses of INa can be adaptive considering the different life
styles of the two species.

In contrast to
other voltage-dependent ion currents, ICaL and IKs seem
to be more resistant to chronic temperature changes (viitteet). The absence of
acclimatory response in ICaL density to temperature  may be related to Ca2+ influx
through Ca2+ channels, which is relatively independent on
temperature (Kim et al., 2000; Shiels et al., 2000; Shiels et al., 2006). However,
seasonal acclimatization changes the density of ICa in ventricular
myocytes of crucian carp; ICaL was bigger in summer than winter fish
(Vornanen and Paajanen, 2004).

changes (or constancy) of ion current densities are often associated with
increased expression of the respective ion channel gene transcripts. This is
consistent with finding that the density of cardiac ion currents is mainly
regulated at transcriptional level (Rosati and McKinnon).  This conclusion applies to fish cardiac erg
(IKr), Kir2 (IK1), Nav1 (INa) and KCNQ1 (IKs)
channels. (Haverinen and Vornanen
2007, Tikkanen et al. 2017). (Hassinen et al., 2007; Hassinen et al., 2008;
Hassinen et al., 2014). (Hassinen
et al., 2008; Hassinen et al., 2014; Vornanen and Hassinen, 2016). (Hassinen et
al. 2008). (Hassinen et al., 2007; Hassinen et al.,

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