From wake dynamics to energy consumption in free-swimming biohybrid robotic jellyfish: a multiscale analysis

Abstract

Measuring energy consumption of marine organisms often requires enclosing the animal in a small, sealed chamber to quantify changes in oxygen concentration of the surrounding water. This can limit measurements of free-swimming organisms by introducing recirculation effects and movement restrictions. We experimentally investigate free-swimming jellyfish energy consumption at two scales: individual pulses and multi-day swimming. Prescribing pulse frequency using onboard microelectronic swim controllers enables comparison of wake energetics across stroke frequencies while allowing continuous swimming. On the microscale, we quantified pulse wake hydrodynamics using three-dimensional Particle Image Velocimetry. Electrical stimulation increased posterior wake energy loss 2.9 times compared to unstimulated jellyfish due to higher pulse rates and altered kinematics. On the macroscale, we used a 6-meter, 13,600-liter tank and tracking-based feedback control to enable continuous swimming against flow over 2.55 km without encountering tank limits. A non-invasive technique quantified changes in 3D morphology without feeding, and volume changes were converted to energy consumption using elemental analysis. Free-swimming, electrically stimulated animals consumed 2.5 times more energy than similarly stimulated animals in a constrained environment, consistent with hydrodynamic and behavioral differences including increased speed and reduced boundary effects. These results suggest hydrodynamic drag may be underrepresented in confined experimental studies.