Temperature blood circulation, cardiac function, and thus heart

Temperature is the environmental master
factor which has a substantial effect on the growth, nutrition, reproduction,
distribution and behaviour of ectothermic fish. Increases and decreases of
ambient water temperature will be reflected on the cardiac function in teleost
fish which considers as a key physiological variable in environmental
adaptation and acclimation of aquatic vertebrates via delivery oxygen and
nutrients to tissue cells and providing homeostatic balance between body parts.
Also, temperature determines the metabolic rate, sets demands on blood
circulation, cardiac function, and thus heart rate (fH) which
is the main regulatory for cardiac output and circulation in fishes with
temperature changes (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). To this end, temperature of water
environemnt acts as a leading factor which control the boundary of habitats of
aquatic organsms (Skelly, 2010).

Climate warming
is considered to be the most serious environmental threat for freshwater
ecosystems and their biodiversity. According to the current scenarios, the
annual mean temperature in Finland is projected to rise by 2–5°C and 2–7°C by
the 2050s and 2080s, respectively. The duration of ice cover in lakes will
become shorter, winters will be milder and extreme temperature peaks are likely
to be higher and occur more often. Changes of these magnitudes are likely to
seriously affect fish populations in Finland. For example, the Arctic charr (Salvelinus
alpinus), a cold-water salmonid species, faces a real heat threat
especially in the shallow lakes of northern Finland (Lehtonen, 1998; Heino et
al., 2009). Unlike the Arctic charr, which has a narrow thermal tolerance
window, the roach tolerates a much wider range of temperatures. Putatively, the
roach may be one of the fish species which may benefit from the warming waters;
therefore its abundance in Finnish lakes and coastal waters may increase with
significant impact on those ecosystems. Jeppesen et al. (2012) reviewed the
impacts of climate warming on fish data series from 24 European lakes, included
2 Finnish lakes, with annual temperature increase of about 0.15-0.3°C per decade where
profound changes have occurred in fish assemblage
composition, biomass, abundance, body size and/or age structure and a shifted
towards higher dominance of eurythermal species with decreasing in the
abundance of cold-stenothermal species. Strongly response of fishes to the
warming makes them as indicator for detecting and documenting climate-induced
modifications on freshwater ecosystems.

As ectotherms,
Fishes can acclimatize and adjusting their physiological and biochemical
processes during seasonal and daily thermal variations or vertical movements
through the water column (Matthews and Berg 1997, Wood and McDonald 1997). In north-temperate
latitudes, fish live and tolerate near-zero temperatures, while the limitation
of upper thermal tolerance and plasticity different between species (Bennett
and Beitinger, 1997; Beitinger and Bennett, 2000). According to the upper
thermal tolerance, fish can be classified into 3 groups, stenothermal,
mesothermal and eurythermal fish. Stenothermic fish have ability to tolerate
narrow range of temperatures as fish in the Southern Ocean which living under
the constant cold and tolerate narrow range of temperatures usually less than
10 degrees (Verde et al., 2006; Franklin et al., 2007). Contrary, some
eurythemial fish have ability to tolerate wide range of temperatures between 0°C to 40°C (Bennett and Beitinger, 1997; Rantin et al., 1998; Beitinger and
Bennett, 2000) as crucian carp (0-36°C; Horoszewicz, 1973) and
roach (0-33°C; Cocking, 1959). Between both stenothermal and eurythermal fish,
fish with intermediate thermal tolerance range called as mesothermal fish as salmonid
fish which tolerate range of temperatures from about 0°C to
22-28°C and classified as mesothermic fish (Elliott and Elliott, 2010).

characteristics of animals (phenotypes) are not fixed within individuals, but
include a plastic component. Hence, animals can remodel their physiology to
compensate for the effects of temperature variation via a process of thermal
acclimation (also called physiological plasticity) and thereby confer resilience
to climate change. Knowledge on the physiological plasticity of ectotherms and
its molecular and genetic basis is crucial when predicting the effects of
global warming on animal populations. Importantly, the electrophysiological
phenotype of the ectothermic heart is flexible, so that function of heart and
nerves is reversibly changed between cold and warm seasons. The change
phenotype involves a number of changes ion channel structure and composition
and in thermal properties of ion currents. Physiological thermal plasticity of
fish heart is crucial to maintain contractility and to avoid disturbances in
electrical excitability that should be sensitive to temperature changes to
produce temperature-dependent acceleration and deceleration of heart rate (fH)
and coordinate changes in conduction rate of action potential (AP) over the
heart (Hassinen et al., 2007; Haverinen and Vornanen, 2009; Vornanen et al.,
2014; Badr et al., 2016).
Increases in beating frequency reduce duration and plateau height of the fish
cardiac AP (Harwood et al., 2000), and similarly acute changes in temperature
cause profound changes in the shape of cardiac AP, including atrial and
ventricular myocytes as well as pacemaker cells (Harper et al., 1995; Haverinen
and Vornanen, 2007; Vornanen et al., 2014; Lin et al., 2014). The shape and
duration of the AP is highly temperature-sensitive and appears to play an
important role in thermal acclimation of freshwater teleost cardiomyocytes
(Bers, 2001; Haverinen and Vornanen, 2009, Galli et al., 2009). Acute changes
of temperature extends also to include ion currents (K+, Na+
and Ca2+), which control AP, and molecular composition of ion
channels. Generally, temperature virtually affects all levels of biological
organization from molecular diffusion to biochemical reactions, membrane
function and organ function which constitute the whole organism (Kalinin
et.al., 2009).


1.6.1  Effect of temperature on heart rate (fH)


The rhythmicity of the heart is originated
by pacemaker cells in the region between sinus venosus and atrium. Thermal
placticity is variable between fish species and may limit the adaptability of
fishes in surviving with predicted climate warming (Somero, 2010). Both of
heart rate (fH) and the stroke volume (SV) determine the performance
of the heart and result in cardiac output. In exercising fish, changes in
cardiac output are achived by increases in both SV and fH,
while fH is the main factor in regultation the cardiac output
during temperature changes (Randall, 1982; Gollock et al., 2006; Steinhausen et
al., 2008; Mendonça and Gamperl, 2010; Farrell and Smith, 2017). In most of fish,
increase of temperature increases fH, e.g. from a few number
heartbeats per minute (bpm) to a maximum fH of 70-120 bpm (Lillywhite
et al., 1999; Gollock et al., 2006; Mendonça and Gamperl, 2010). However, the
maximum fH can be increased to 300 bpm at high temperatures in
zebrafish and frillfin goby (Bathygobius soporator) (Rantin et
al., 1998; Lin et al., 2014; Sidhu et al., 2014; Vornanen and Hassinen, 2016). Decrease
in temperature from 25° C to 10° C resulted in reducing the fH
of yellowfin tuna (Thunnus albacares) from 106 bpm to 20 bpm (Blank
et.al., 2002). Similarly, Nile tilapia (Oreochromis niloticus) which
acclimated to 35° C follwed by acute temperature decline to 15° C
(Maricondi-Massari et.al., 1998). In contrast, fH in cold
acclimated Pacu (Piaractus mesopotamicus) and goldfish (Carassius
auratus) was higher than that in warm acclimated fish (Morita and Tsukuda,
1995; Aguair et.al., 2002). These results indicate that the cardiac
contractility (fH) alternations following temperature changes
are not uniform among teleosts and the effects of temperature acclimation on
the heart rate are species-specific dependent.

Changes in
temperature cause compensatory changes in fH which also require
modifications in the duration of pacemaker, atrial and ventricular APs to
maintain a proper balance between the durations of systole (cardiac
contraction) and diastle (cardiac relaxation) (Vornanen, 2016). In seasonal
acclimated plaice (Pleuronectes platessa) and thermal acclimated rainbow
trout at 4°C, low temperatures induce increrases in fH  by shortening in the pacemaker APD without
changes in the rate diastolic depolarization (Harper et al., 1995; Haverinen
and Vornanen, 2007). In some other fishes, increases in fH
induced by cold temperatures is due to shortening of atrial and ventricular APs
(Haverinen and Vornanen, 2009, Hassinen et al., 2014; Abramochkin and Vornanen,

temperature changes cause different types of arrhythmias in fish hearts appeare
when temperature approaching or exceeding the break point temperature (TBP)
the upper thermal tolerance of fH. Cardiac arrhythmias
reported in fish hearts as missed beats, bradycardia, and bursts of rapid
beating, and finally 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 action potential (AP)


Acute temperature changes significantly change
the duration and shape of pacemaker, atrial and ventricular APs of fish hearts
by altering the flow of inward and outward currents via the SL in
temperature-dependent manner (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). APD must inversly correlate with fH to allow
sufficient time for systole and diastole durations, otherwise diastole will
disappear under high fH, i.e, increasing in temperature
increases fH and decreases APD. In exercise and active fishes
(as tunas) and tropical fishes (as zebrafish) have higher fH
and shorter APD in comparison with dormant fishes (as crucian carp) or fishes
live in cold polar waters (as navaga). The shape and duration of fish cardiac
APs and the underlying ion currents are highly sensitive to temperature changes
and crucial in thermal acclimation or acclimatization of both freshwater and
marine teleosts to seasonal temperature regimes (Haverinen and Vornanen, 2009;
Galli et al., 2009; Hassinen et al., 2014; Abramochkin and Vornanen, 2015;
Vornanen and Hassinen, 2016).