Omnidirectional propulsion in a metachronal swimmer

PLoS Comput Biol. 2023 Nov 17;19(11):e1010891. doi: 10.1371/journal.pcbi.1010891. eCollection 2023 Nov.

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.

MeSH terms

  • Animals
  • Biomechanical Phenomena
  • Cetacea
  • Fishes*
  • Swimming*

Grants and funding

This work was supported by the National Academies Keck Futures Initiative (#DBS5 to MLB); the National Science Foundation (NSF CBET-2120689 to MLB); and the Consejo Nacional de Ciencia y Tecnologia (CONACYT) of Mexico (#2019-000021-01EXTF-00633 to AHA). MLB received salary from NSF. CONACYT and NSF both provided a partial graduate assistantship for AHA. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.