Invertebrate Athletes: Trade-Offs Between Transport Efficiency and Power Density in Cephalopod Evolution

Abstract

Jet propulsion concentrates muscle power on a small volume of high-velocity fluid to give high thrust with low Froude efficiency. Proponents are typically escape artists with high maintenance costs. Nonetheless, oceanic squids depend primarily on jets to forage over large volumes of relatively unproductive ocean (low power density, Wm−3). A survey of locomotor performance among phyla and along an ‘evolutionary continuum’ of cephalopods (Nautilus, Sepia, Loligo and Illex) suggests that increasing speed and animal power density are required if animals are to compete effectively in environments of decreasing power density. Neutral buoyancy and blood oxygen reserves require unproductive volume, keeping drag high. Undulatory fins increase efficiency, but dependence on muscular hydrostats without rigid skeletal elements limits speed. Migratory oceanic squids show a remarkable range of anatomical, physiological and biochemical adaptations to sustain high speeds by maximizing power density. Muscle mitochondrial density increases 10-fold, but metabolic regulation is realigned to optimize both aerobic and anaerobic capacity. The origins of these adaptations are examined (as far as possible, and perhaps further) along the continuum leading to the most powerful invertebrates.