Aspects of the physiology and anatomy of cardiac and skeletal muscles in South Polar notothenioid fish

Abstract

Aspects of the physiology and anatomy of cardiac and skeletal muscle in south polar notothenioid fish have been investigated. Relative ventricle weights for the haemoglobinless Chaenocephalus aceratus (family Channichthyidae) were approximately three times greater than for sympatric 'red-blooded' species. The ventricle in the channichthyid was 'sac-like' in shape and had an entirely trabecular myocardium: these characteristics were associated with low maximum myocardial power outputs (1.46mW(g ventricle weight) ⁻¹). The blood supply to the ventricle was through the venous lacunary circuit and vessels in the subepicardium. The myoglobin-poor ventricular myocardium in C.aceratus was composed of myocytes and granulated non-contractile cells. Myocardial cytochrome oxidase activity (34 μmoles g⁻¹min⁻¹) at O°C was similar to that of warmer-water species with myoglobin-rich ventricles. This suggests that the channichthyid has achieved compensation for the rate depressing effects of the low temperatures and low myoglobin concentrations on oxidative metabolism. Morphometric analyses of the myocytes in C.aceratus indicated that they had higher mitochondrial (0.43) and lower myofibrillar (0.31) volume densities than other teleosts. It was proposed that the proliferation of mitochondria serves to maintain high aerobic capacities by reducing oxygen diffusion distances between the lacunae and the myocytes. The anatomy of the pectoral fin muscles in N.neglecta (family Nototheniidae) has been described. Six muscles (2.49% of total body weight) articulated the fin blade. These were composed of a core of small diameter fibres (18-99μm) which stained intensely for markers of aerobic metabolism. Overlying these was a layer of larger diameter fibres (24-156μm) which stained poorly for these markers. The two fibre types were also differentiated on the basis of their mechanical properties: demembranated preparations of the larger diameter fibres generated approximately twice the tensions and had twice the unloaded contraction velocities of the small diameter fibres. Despite these differences however, the fibres could not easily be differentiated on the basis of the pH stabilities of their myosins. At 1°C the maximum isometric tension (Po) generated by both pectoral fibre types in N.neglecta demonstrated incomplete temperature compensation compared to published values for homologous fibres in warm-water teleosts. Unloaded contraction velocity (Vmax) was not temperature compensated. In addition to Po, adaptive modifications in the curvature of the force-velocity curves were identified in the nototheniid which served to enhance power output at low temperatures. Between -5 and +10°C Po was relatively temperature independent (R₁₀ = approximately 1.2) whereas the temperature coefficent of Vmax was high (Q₁₀ = approximately 2). Following activations in excess of 12°C both fibre types failed to relax completely. This suggests that adaptations in the contractile proteins which conferred high power outputs at low temperatures were associated with a limitation in the temperature range over which they could maintain function. Simultaneous measurements were made of force generation and myofibrillar ATP hydrolysis during isometric contractions in demembranated white trunk fibres isolated from teleosts adapted to different thermal environments. ATP hydrolysis was quantified using a novel technique which allowed the fibres to be activated in the presence of an ATP regenerating system based on phosphocreatine and creatine phosphokinase. ATP activity was determined by measuring the increase in free creatine in the activating solution. The results obtained indicated that the economy of contraction (tension/ATP hydrolysed) was substantially higher in the fibres from Notothenia neglecta than those from warmer-water species at their preferred body temperatures.