Squid (Lolliguncula brevis) were exercised in a tunnel respirometer during a stepwise increase in water velocity in order to evaluate the anaerobic threshold, i.e. the critical swimming speed above which anaerobic metabolism contributes to energy production. The average anaerobic threshold was found at speeds of 1.5-2 mantle lengths s-1. Above this velocity, alpha-glycerophosphate, succinate and octopine started to accumulate in the mantle tissue. ATP levels fell and phospho-L-arginine was progressively depleted, while the levels of glucose 6-phosphate and inorganic phosphate rose. The finding of a simultaneous onset of anaerobic metabolism in the cytosol and the mitochondria indicates that a limited oxygen supply to the mitochondria elicits anaerobic energy production. This finding is opposite to the situation found in many other vertebrate and invertebrate species, in which energy requirements in excess of aerobic energy production are covered by anaerobic metabolism, with mitochondria remaining aerobic. In L. brevis, swimming at higher speeds is associated with a small factorial increase in metabolic rate based on a high resting rate of oxygen consumption. Pressure recordings in the mantle cavity support this finding, indicating a high basal level of spontaneous activity at rest and a small rise in mean pressure at higher swimming velocity. Bursts of higher pressures from the jet support elevated swimming speeds and may explain the early transition to anaerobic energy production which occurs when pressure amplitudes exceed 1.2-1.5 kPa or when mean pressure rises above 0.22-0.25 kPa. The finding of mitochondrial hypoxia at a low critical speed in these squid is interpreted to be related to their life in shallow coastal and bay waters, which limits the necessity to maintain high swimming velocities. At increased swimming velocities, the animals oscillate between periods of high and low muscular activity. This behaviour is interpreted to reduce transport cost and to permit a longer-term net use of anaerobic resources when speed exceeds the critical value or when the squid dive into hypoxic waters. The simultaneous onset of anaerobic metabolism in the cytosol and the mitochondria emphasizes that squid generally make maximal use of available oxygen under resting conditions, when their energy requirements are the highest among marine invertebrates.
Squid (Lolliguncula brevis) life in shallow waters: oxygen limitation of metabolism and swimming performance.
E Finke, H O Pörtner, P G Lee, D M Webber; Squid (Lolliguncula brevis) life in shallow waters: oxygen limitation of metabolism and swimming performance.. J Exp Biol 1 April 1996; 199 (4): 911–921. doi: https://doi.org/10.1242/jeb.199.4.911
Download citation file:
Advertisement
Cited by
In the field: an interview with Martha Muñoz

Martha Muñoz is an Assistant Professor at Yale University, investigating the evolutionary biology of anole lizards and lungless salamanders. In our new Conversation, she talks about her fieldwork in Indonesia, Costa Rica, the Dominican Republic and the Appalachian Mountains, including a death-defying dash to the top of a mountain through an approaching hurricane.
Graham Scott in conversation with Big Biology

Graham Scott talks to Big Biology about the oxygen cascade in mice living on mountaintops, extreme environments for such small organisms. In this JEB-sponsored episode, they discuss the concept of symmorphosis and the evolution of the oxygen cascade.
Propose a new Workshop
-GSWorkshop.png?versionId=3846)
Our Workshops bring together leading experts and early-career researchers from a range of scientific backgrounds. Applications are now open to propose Workshops for 2024, one of which will be held in a Global South country.
Manipulation of mitochondrial function affects red carotenoid metabolism in a marine copepod

Tigriopus californicus copepods with the most powerful mitochondria are the brightest red, providing an honest and direct link between the attractiveness of a creature and their metabolic prowess.
The physiological cost of colour change

In their Review, Ateah Alfakih, Penelope Watt and Nicola Nadeau discuss the energetic cost of colour change and highlight how this can be avoided or lessened in animals that change colour rapidly or slowly.