Environmental and functional limits to muscular exercise and body size in marine invertebrate athletes

Many similarities exist between the key characteristics of muscular metabolism in marine invertebrates and those found in vertebrate striated muscle, even though there are important phosphagens and glycolytic end products that differ between groups. Lifestyles and modes of locomotion also vary extremely among invertebrates thereby shaping the pattern of exercise metabolism. In accordance with the limited availability of integrated ecological and physiological information the present paper reports recent progress in the exercise physiology of cephalopods, which are characterized by high rates of aerobic and anaerobic energy turnover during high velocity hunts or escapes in their pelagic environment, and a sipunculid worm, which mostly uses anaerobic resources during extended marathon-like digging excursions in the hypoxic marine sediment. Particular attention is paid to how lifestyle and oxygen availability in various marine environments shapes the use and rates of aerobic and anaerobic metabolism and acidosis as they depend on activity levels and energy saving strategies. Whereas aerobic scope and, accordingly, use of ambient oxygen by blood oxygen transport and skin respiration is maximized in some squids, aerobic scope is very small in the worm and anaerobic metabolism readily used upon muscular activity. Until recently, it was widely accepted that the glycolytic end product octopine, produced in the musculature of these invertebrates, acted as a weak acid and so did not compromise acid-base balance. However, it has now been demonstrated that octopine does cause acidosis. Concomitant study of tissue energy and acid-base status allows to evaluate the contribution of glycolysis, pH and free ADP accumulation to the use of the phosphagen and to the delayed drop in the Gibb's free energy change of ATP hydrolysis. The analysis reveals species specific capacities of these mechanisms to support exercise beyond the anaerobic threshold. During high intensity anaerobic exercise observed in squid, the levels of ATP free energy change finally fall to critical minimum levels contributing to fatigue. Maintenance of sufficiently high energy levels is found at low but extended rates of anaerobic metabolism as observed in the long term digging sipunculid worm. The greatest aerobic and anaerobic performance levels are seen in squid inhabiting the open ocean and appear to be made possible by the uniform and stable physicochemical parameters (esp. high O(2) and low CO(2) levels) that characterize such an environment. It is suggested that at least some squid operate at their functional and environmental limits. In extremely different environments, both the worm and the squids display a tradeoff between oxygen availability, temperature, performance level and also, body size.