Metachronal coordination enables omnidirectional swimming via spatially distributed propulsion

Abstract

Aquatic organisms often employ maneuverable and agile swimming behavior to escape from predators, find prey, or navigate through complex environments. Many of these organisms use metachronally coordinated appendages to execute complex maneuvers. However, though metachrony is used across body sizes ranging from microns to tens of centimeters, it is understudied compared to the swimming of fish, cetaceans, and other groups. In particular, metachronal coordination and control of multiple appendages for three-dimensional maneuvering is not fully understood. To explore the maneuvering capabilities of metachronal swimming, we combine 3D high-speed videography of freely swimming ctenophores (Bolinopsis vitrea) with reduced-order mathematical modeling. Experimental results show that ctenophores can quickly reorient, and perform tight turns while maintaining forward swimming speeds close to 70% of their observed maximum -- performance comparable to or exceeding that of many vertebrates with more complex locomotor systems. We use a reduced-order model to investigate turning performance across a range of beat frequencies and appendage control strategies, and reveal that ctenophores are capable of near-omnidirectional turning. Based on both recorded and modeled swimming trajectories, we conclude that the ctenophore body plan enables a high degree of maneuverability and agility, and may be a useful starting point for future bioinspired aquatic vehicles. Author summaryMetachronal swimming--the sequential, coordinated beating of appendages arranged in a row-- exists across a wide range of sizes, from unicellular organisms (micrometers) to marine crustaceans (tens of centimeters). While metachronal swimming is known to be scalable and efficient, the level of maneuverability and agility afforded by this strategy is not well understood. This study explores the remarkable 3D maneuverability of ctenophores (comb jellies), and the appendage control strategies they use to achieve it. Ctenophores have eight rows of appendages (instead of the one or two found in crustaceans and other organisms). This higher number of appendages, their distribution along the body, and the independent frequency control between paired rows enables near-omnidirectional swimming and turning performance, placing ctenophores among the most maneuverable swimmers. We use experiments and mathematical modeling to explore both the real and theoretical performance landscape of the ctenophore body plan, and show that ctenophores are capable of executing tight turns at high speeds in nearly any plane. This omnidirectional swimming capability gives insight into the ecology and behavior of an important taxonomic group, and shows the potential of metachronal swimming as a source of design inspiration for robotic vehicles (particularly those that must navigate complex environments).