Environmental constraints and the physiology of performance in squids

Abstract

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. Onc 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~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 arc 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.

Impacts of hypoxia on the structure and processes in pelagic communities (zooplankton, macro-invertebrates and fish)

“…Catches of squid have tripled during the last 30 years (MoralesBojorquez et al, 2001;FAO, 2010a) suggesting an increasing role in pelagic foodwebs of neritic and oceanic ecosystems. Squid seems to be more tolerant against low oxygen than many other pelagic organisms, even though their burst swimming method requires more energy than other modes of locomotion, such as swimming in fish (Pörtner and Zielinski, 1998). Their oxygen consumption rises during exercise to fivefold above resting level (Hoeger et al, 1987).…”

Biological Impact of Elevated Ocean CO2 Concentrations: Lessons from Animal Physiology and Earth History

“…A look at the special metabolic and respiratory design of squid explains why these creatures are so sensitive to ambient CO 2 fluctuations (Pörtner and Zielinski, 1998). In contrast to the low metabolic rate associated with undulatory swimming in fish, the squid's oxygen demand is much higher due to their less efficient mode of swimming by jet propulsion (O'Dor and Webber, 1986).…”

Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals

“…Both T cI and T cII vary depending on environmental temperatures at various latitudes and seasons. (modified after Sommer et al 1997;Pörtner and Zielinski 1998;van Dijk et al 1999;Frederich and Pörtner 2000) and demand which leads to a drop in aerobic scope, transition to anaerobic metabolism and finally collapse of higher physiological function in fully aerated environments. Insufficient capacity of ventilation or circulation would not only be the cause of the mismatch between oxygen uptake and demand at extreme temperatures but vice versa, ventilatory or circulatory organs may also be the first to experience the sequence of limited aerobic scope, oxygen deficiency, anaerobiosis and energetic failure.…”