Environmental constraints and the physiology of performance in squids
The highly active squid which inhabit the pelagic zones of continental seas are characterized by high energy requirements and have been termed invertebrate athletes. In this paper, the physiological and biochemical background of muscular performance in squid from different environments is reviewed and the physiological and environmental factors limiting performance levels are addressed. One important factor is the highly concentrated haemocyanin which, in ommastrephid squid, and by virtue of their extreme pH dependence, helps to load oxygen efficiently in the gills and unload it fully into the tissues. Squid regulate their extracellular pH more efficiently than intracellular pH, so protecting the haemocyanin from fatal pH changes. However, a large proportion of the oxygen requirement in the mantle muscle must still be provided by oxygen uptake through the skin. Anaerobic mechanisms become involved beyond critical swimming speeds once oxygen supply to mitochondria becomes limiting. Onset of anaerobiosis also characterizes the limits of long-term tolerance to progressive hypoxia at a critical P(O2) and to high, above-critical temperatures. In general, anaerobic energy production reflects an inability to meet oxygen demand and indicates transition to a time-limited situation. The development of energy-saving locomotion strategies therefore shifts critical thresholds and extends tolerance periods in species exposed to environmental extremes, typically in coastal areas. There, negatively buoyant squid make greater use of the fin for economical swimming, which is also advantageous because of the complexity of the environment. In Lolliguncula brevis, the rate at which anaerobic resources are used above the critical swimming velocity is minimized by oscillating between periods of high and low pressure jets, thereby extending the period during which the animal can dive into hypoxic or warm water. However, only jet propulsion can economically attain the high velocities necessary in the open sea. Accordingly, the highest performance levels are seen in squid inhabiting the open sea, and they are only made possible by the uniform environmental parameters. Some squid may be able to operate at their functional and environmental limits, revealing a trade-off between oxygen availability, temperature, performance level and, possibly, body size.