Temperature
Temperature has quite rightly been termed the `ecological master factor' (Brett, 1971
) as it has a profound effect on the physiology of all ectothermic animals. Nevertheless, it is well known that fish, like other ectotherms, can compensate for the direct effects of temperature on physical processes and enzymatic reaction kinetics through temperature acclimation or acclimatization. Here we focus primarily on the rainbow trout Oncorhynchus mykiss to illustrate cardiac plasticity in response to temperature change.
Salmonids have adapted to exploit the cold water habitats created by retreating glaciers, despite the fact that optimum temperatures for maximum cardiac performance, aerobic scope and swimming ability are commonly around 15–18°C and preferred temperatures typically range from 12 to 18°C (McCauley and Huggins, 1979; Jobling, 1981). Thus, it is perhaps not surprising to find that cardiac function in rainbow trout has a rather low sensitivity to temperature change. Indeed, temperature acclimation between 5 and 18°C results in Q10 values in the range 1.2–1.4 for maximum cardiac output (
max) and maximum power output (POmax) for rainbow trout (Graham and Farrell, 1989; Keen and Farrell, 1994), rather than Q10 values of around 2 if there had been no compensation.
The ability to almost maintain max and POmax across a broad temperature range clearly involves cardiac plasticity that provides advantages to fish that inhabit an environment with fluctuating temperatures. The mechanisms behind this cardiac plasticity in response to temperature are partially understood. For example, exposure to a 10°C decrease in temperature for 3–4 weeks increases relative ventricular mass by 20–40%, but decreases the proportion of compact myocardium by 15–30% (Farrell et al., 1988; Graham and Farrell, 1989). A larger ventricular muscle mass compensates for a cold-temperature-induced decrease in contractility, thereby helping maintain stroke volume (VS), and pressure development. Implicit in this argument is that a decrease in contractility negatively affects end-systolic volume of the ventricle, which in trout is normally very small. At warmer temperatures, ventricular mass could be relatively smaller while maintaining the same because, in addition to improved force of contraction, rates of ventricular contraction and relaxation are faster. These latter effects would increase the time available for cardiac filling, and may compensate for the effect of increased heart rate on end-diastolic volume. Cardiac enlargement, however, is apparently dependent on other factors beside temperature, because rainbow trout held on a 12 h:12 h light:dark photoperiod show either no or a smaller degree of cardiac enlargement ( temperatures (Keen et al., 1993; Keen and Farrell, 1994; Sephton and Driedzic, 1995; Aho and Vornanen, 2001). Although we know little about what these environmental and physiological factors might be, recent work by Tiitu and Vornanen (2003) suggests that cold/seasonal cardiac enlargement may be partially related to thyroid state. Thyroid hormones affect many physiological functions in fishes (e.g. osmoregulation, nitrogen excretion, morphological changes associated with smoltification, muscle growth etc.), and these authors found that hypothyroidism was associated with increases in heart size and heart rate in rainbow trout. The involvement of hypertrophic or hyperplastic myocardial growth in cold/seasonal cardiac enlargement is presently unresolved (Driedzic et al., 1996), although hypertrophy is a well-documented compensatory response to cold temperature in tissues such as the liver (Kent and Prosser, 1985).
The intrinsic cardiac pacemaker rate is also reset with cold acclimation, with heart rate (fH) being higher than it would be following an acute decrease in temperature. This elevation in fH, which is obviously important in maintaining , involves alterations to membrane ion channel function and density, the details of which have been recently discovered and reviewed (Vornanen et al., 2002a,b). For example, the repolarizing K+ currents (Ik), which affect the shape and duration of the action potential (AP), are altered in cold-acclimated rainbow trout and this partially compensates for a cold-induced prolongation of the AP. Specifically, the density of the inward rectifier potassium current, Iki, is depressed in the ventricle, while that of the delayed rectifier current, Ikr, is strongly increased: the net effect is that AP duration and presumably the refractoriness of the heart are shortened.
Similarly, the delivery of calcium to troponin C, which initiates the contractile event and regulates the strength of cardiac contraction, is clearly plastic in fish and responds to temperature. Calcium entry into cardiomyocytes via the L-type Ca2+ channel (ICa) plays an important role in cardiac contractility, including triggering the release of intracellular Ca2+ from the sarcoplasmic reticulum (SR) and directly activating the myofilaments. Ion flow through cardiac L-type Ca2+ channels in mammals, and surprisingly also rainbow trout, is extremely temperature sensitive, with peak current having a Q10 of 1.8–2.1 for acute temperature changes (Kim et al., 2000; Shiels et al., 2000). However, in rainbow trout, a slowing of channel inactivation and a prolongation of the AP counteracts the depressive effect of cold temperature on peak ICa such that the net calcium charge transfer is essentially independent of an acute temperature change (Shiels et al., 2000). With cold-acclimation the AP is shortened through the plasticity of the sarcolemmal K+ channels (noted above), and although the density of ICa when measured at room temperature is the same for cold- and warm-acclimated rainbow trout and carp, the rate of ICa inactivation is greater for the cold-acclimated fish (Vornanen, 1998). Given the temperature dependent decrease in myofilament Ca2+ sensitivity, it seems likely that a compensatory increase in Ca2+ from another source is needed to maintain the same force of contraction at low temperature (see Vornanen et al., 2002a,b). In this regard, cold-induced proliferation of SR (another source of activator Ca2+ for contraction) has been observed and cold-acclimated fish respond more robustly to ryanodine (an SR Ca2+ release agonist), especially when the tissue is acutely warmed (see Shiels et al., 2002). Thus, to activate muscle contraction, a larger SR capacity could compensate for a smaller SL Ca2+ trigger. However, the possibility that cold-induced hyperplastic cardiac growth could enhance the myocyte to surface area to volume ratio, and thus augment sarcolemmal-dependent processes, has not been thoroughly explored.
Extrinsic modulation of the heart is also altered by temperature acclimation, and in this regard certain cellular transduction mechanisms are known to show temperature-dependent plasticity. Wood et al. (1979) showed that cholinergic inhibitory tonus in rainbow trout is more important in setting routine heart rate at cold temperatures, while adrenergic excitatory tonus is relatively more important at high temperature. However, temperature effects on the adrenergic signal transduction pathway that controls ventricular contractility appear to be opposite to those seen for heart rate. In particular, the rainbow trout myocardium becomes more responsive to ß-adrenergic stimulation with cold acclimation. This is due to an increase in the density of SL ß-adrenoceptors (Keen et al., 1993) and an upregulation of the secondary messenger cascade (Keen, 1992), and the former response clearly needs further study to determine whether receptors are being sequestered and cycled to the membrane, or whether genes are being turned on to make more receptors. ß-adrenergic stimulation shortens the AP and stimulates ICa (Shiels et al., 2002). In fact, the possibility exists that tonic adrenergic stimulation may be critical for adequate L-type Ca2+ channel function at cold temperatures in rainbow trout (Shiels et al., 2004), as well as proper atrio–ventricular coordination (Graham and Farrell, 1989).
While much has been learned about the mechanistic basis for cardiac plasticity in rainbow trout, limited studies with other fish species clearly point to alternative patterns of cardiac plasticity. For example, the hearts of Arctic charr Salvelinus alpinus reared at 15°C are 15–30% larger, not smaller, than the hearts of fish reared at 5°C (Ruiz and Thorarensen, 2001). Carp are an extremely eurythermal family, and winter dormancy in Cyprinus carpio is associated with a suppression of routine cardiac power output (Q10
4) through intrinsic mechanisms rather than cholinergic suppression of cardiac activity (J. A. W. Stecyk and A. P. Farrell, unpublished data). Conversely, Carassius carassius, which survives winter anoxic conditions by fermenting glucose to alcohol, maintains cardiac activity (J. A. W. Stecyk et al., unpublished data) despite increased cardiac refractoriness (Tiitu and Vornanen, 2001). The ability of the Pacific bluefin tuna Thunnus orientalis heart to maintain cardiac pumping at cold temperatures that are refractory to hearts from other tuna species appears to be directly related to a high SR Ca2+ ATPase activity, and this cardiac feature may be a primary adaptation that allows this species to forage to deeper and colder depths (Blank et al., 2004). Similarly, the burbot Lota lota, which also remains active in deep lakes during winter, has an unusually high SR Ca2+-release at 1°C, which is reduced at warmer acclimation temperatures (Tiitu and Vornanen, 2002). The idea that the pattern of cardiac plasticity for cold-active fishes differs from cold-inactive fishes is also supported by data on thermal compensation of heart rate and twitch kinetics in yellow perch Perca flavescens vs sea raven Hemitripterus americanus (Driedzic et al., 1996), and by data on the cardiac responses of sympatric bass species with differences in winter activity (Cooke et al., 2003).
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