Aerobic and anaerobic scaling in fish

Abstract

The maximum metabolic rate of fish, measured during aerobic swimming, scales according to a mass exponent ≥ 1.0. This is not in accord with the negative allometry of aerobic metabolism predicted by the scaling of oxygen uptake and delivery. An analysis of the tissue-specific distribution of aerobic capacity in fish indicates that only a small proportion, perhaps 10-20%, of total capacity occurs in the red muscle tissue used during aerobic swimming. This is in sharp contrast to the situation in mammals where the majority of whole-body aerobic capacity is found in the skeletal muscles. Because of its large mass, the characteristically anaerobic white muscle tissue of fish contains most of the whole-body aerobic capacity. This aerobic potential may be responsible for oxygen consumption rates following exercise (oxygen debt) which are higher than during aerobic swimming. Total viscera aerobic capacity is also higher than red muscle capacity for small, i.e. fast-growing, individuals. This is aerobic capacity associated with food processing, and its negative allometry can account for the observation that postprandial elevations in oxygen consumption can exceed the active metabolic rate for small fish but not for large ones. The use of postprandial metabolic rate as the maximum metabolic rate for small fish should result in a scaling function for maximum metabolic rate which displays the expected negative allometry. Because different physiological activities are responsible for maximum metabolic rate in different sized fish, no single 'use-based' theory (e.g. locomotor muscle power) should be able to account for the scaling of aerobic metabolism. Enzymatic and metabolite evidence indicates positive allometry in the anaerobic potential of fish white muscle. This appears to be the situation for both intraspecific and interspecific scaling. The allometry of anaerobic demand is influenced by (1) higher weight-specific power requirements in larger fish during burst and sprint swimming and (2) decreasing weight-specific aerobic power production by the muscle of larger fish. The swimming of very small (larval) fish appears to be powered primarily by aerobic metabolism even at burst and sprint speeds. This conclusion is based on (1) the scaling of performance at burst and aerobic swimming, (2) comparisons of power requirements and red muscle power output, and (3) the enzyme profiles of larval fish. Increased dependence on anaerobic energy production seems to occur at approximately 1-3 cm. Upper limits to anaerobic metabolism in large fish are constrained by the scaling of glycogen reserves (= L3), which do not increase as fast as the power requirements at burst speeds (=L4.4). More importantly, decreasing aerobic capacity at large sizes results in estimated glycogen restoration times which are prohibitively long (> 10 days). Estimates of daily weight-specific anaerobic energy production, based on glycogen restoration times, decrease by approximately two orders of magnitude with increased size. This expression of anaerobic metabolism indicates, not positive, but rather negative allometry. The scaling of anaerobic metabolism displays characteristics of both positive and negative allometry, which means that it may not be possible to accurately describe it with any general mass exponent. These considerations also suggest that there is an optimal size for the practical exploitation of anaerobic metabolism during locomotion.