A Violation of the Metabolism-Size Scaling Paradigm: Activities of Glycolytic Enzymes in Muscle Increase in Larger-Size Fish

Abstract

The activities (units per gram wet weight of tissue) of two glycolytic enzymes (lactate dehydrogenase [LDH] and pyruvate kinase [PK]) and two citric acid cycle enzymes (citrate synthase [CS] and malate dehydrogenase [MDH]) were measured in epaxial white muscle of different-sized specimens of 13 teleost species. For CS, an enzyme associated with aerobic metabolism, the units of activity per gram muscle decreased with increasing body size, following the scaling pattern characteristically observed for aerobic respiration as a function of body size. The two anaerobically poised enzymes, LDH and PK, exhibited significantly higher activity per gram muscle in larger specimens. The dramatic increases in LDH and PK activities, both in terms of units per gram muscle and units of muscle activity per gram of total fish mass, were analyzed from the standpoint of power requirements for burst-swimming performance, since glycolytic capacity may determine a fish's ability to swim at high relative (body lengths per second) velocities. The scaling of muscle power required for maintenance of identical burst-swimming abilities (in body lengths per second) in large and small individuals of a species, based on calculations of drag scaling with body size and relative swimming velocity, agrees closely with the observed scaling of LDH and PK activity in white epaxial muscle. Brain enzymic activities were examined in three species to determine whether enzyme scaling with body size also occurred in a nonlocomotory tissue. The LDH and PK activities were virtually constant over a wide range of body size in all three species; CS activity exhibited a scaling with body size similar to the relationship found for white muscle CS activity and similar to the relationship expected between respiratory rate and body size. These different enzymic activity scaling patterns for aerobically and anaerobically poised enzymes are discussed in terms of the body-sizedependent aerobic. swimming abilities and body-size-independent anaerobic (burst) swimming abilities of fish. The ecological significance of maintaining size-independent burst-swimming ability, as measured in body lengths per second, is also considered. The contrasting aerobic and anaerobic enzyme scaling patterns found in this study indicate that the metabolic scaling paradigm observed in numerous studies of respiratory metabolism may not be applicable to anaerobic metabolism since different constraints on metabolic rate may apply under aerobic and anaerobic conditions. Limitations on aerobic metabolism may derive from surface-volume relationships and on oxygen transport capacities, i.e., on intertissue relationships. In contrast, limitations on short-term anaerobic metabolism, as used in burst swimming, may involve only intratissue factors, notably glycogen concentration and the activities of glycolytic enzymes like PK and LDH that are instrumental in supplying ATP and in regenerating NAD⁺.