Energy-Information Trade-Offs between Movement and Sensing

Abstract

While there is accumulating evidence for the importance of the metabolic cost of information in sensory systems, how these costs are traded-off with movement when sensing is closely linked to movement is poorly understood. For example, if an animal needs to search a given amount of space beyond the range of its vision system, is it better to evolve a higher acuity visual system, or evolve a body movement system that can more rapidly move the body over that space? How is this trade-off dependent upon the three-dimensional shape of the field of sensory sensitivity (hereafter, sensorium)? How is it dependent upon sensorium mobility, either through rotation of the sensorium via muscles at the base of the sense organ (e.g., eye or pinna muscles) or neck rotation, or by whole body movement through space? Here we show that in an aquatic model system, the electric fish, a choice to swim in a more inefficient manner during prey search results in a higher prey encounter rate due to better sensory performance. The increase in prey encounter rate more than counterbalances the additional energy expended in swimming inefficiently. The reduction of swimming efficiency for improved sensing arises because positioning the sensory receptor surface to scan more space per unit time results in an increase in the area of the body pushing through the fluid, increasing wasteful body drag forces. We show that the improvement in sensory performance that occurs with the costly repositioning of the body depends upon having an elongated sensorium shape. Finally, we show that if the fish was able to reorient their sensorium independent of body movement, as fish with movable eyes can, there would be significant energy savings. This provides insight into the ubiquity of sensory organ mobility in animal design. This study exposes important links between the morphology of the sensorium, sensorium mobility, and behavioral strategy for maximally extracting energy from the environment. An “infomechanical” approach to complex behavior helps to elucidate how animals distribute functions across sensory systems and movement systems with their diverse energy loads.

Author Summary

Animals thrive by sensing their environment and using the information they've gathered to guide their movement. But collecting better information can result in less efficient movement: Bicycling while standing up on the pedals may help you see over obstacles ahead of you, but it causes more air drag, forcing your legs to work harder. Nocturnal weakly electric fish search for prey with their body tilted. This tilting more than doubles the resistance to movement from the water, but because the fish's ability to sense prey improves when tilted, it is better to swim this way. Beyond a certain amount of tilt, the costs of movement become too great. Interestingly, the benefit of tilting is dependent on the shape of the volume around the fish where it detects prey. We also found that if the fish was able to swivel its region of prey sensitivity, like a vision-based animal can shift its gaze, it would save energy. This conclusion helps us understand why animals like us can move our eyes. A Polish folk saying succinctly captures the gist: “He who doesn't have it in the head has it in the legs” (Ten kto nie ma w głowie ma w nogach).