Metachronal Motion across Scales: Current Challenges and Future Directions.

Metachronal motion is used across a wide range of organisms for a diverse set of functions. However, despite its ubiquity, analysis of this behavior has been difficult to generalize across systems. Here we provide an overview of known commonalities and differences between systems that use metachrony to generate fluid flow. We also discuss strategies for standardizing terminology and defining future investigative directions that are analogous to other established subfields of biomechanics. Finally, we outline key challenges that are common to many metachronal systems, opportunities that have arisen due to the advent of new technology (both experimental and computational), and next steps for community development and collaboration across the nascent network of metachronal researchers.

Emergent Metachronal Waves using Tension-Driven, Fluid-Structure Interaction Models of Tomopterid Parapodia.

Metachronal waves are ubiquitous in propulsive and fluid transport systems across many different scales and morphologies in the biological world. Tomopterids are a soft-bodied, holopelagic polychaete that use metachrony with their flexible, gelatinous parapodia to deftly navigate the midwater ocean column that they inhabit. In the following study, we develop a three-dimensional, fluid-structure interaction model of a tomopterid parapodium to explore the emergent metachronal waves formed from the interplay of passive body elasticity, active muscular tension, and hydrodynamic forces. After introducing our model, we examine the effects that varying material properties have on the stroke of an individual parapodium. We then explore the temporal dynamics when multiple parapodia are placed sequentially and how differences in the phase can alter the collective kinematics and resulting flow field.

Neuromechanical wave resonance in jellyfish swimming.

For organisms to have robust locomotion, their neuromuscular organization must adapt to constantly changing environments. In jellyfish, swimming robustness emerges when marginal pacemakers fire action potentials throughout the bell's motor nerve net, which signals the musculature to contract. The speed of the muscle activation wave is dictated by the passage times of the action potentials. However, passive elastic material properties also influence the emergent kinematics, with time scales independent of neuromuscular organization. In this multimodal study, we examine the interplay between these two time scales during turning. A three-dimensional computational fluid-structure interaction model of a jellyfish was developed to determine the resulting emergent kinematics, using bidirectional muscular activation waves to actuate the bell rim. Activation wave speeds near the material wave speed yielded successful turns, with a 76-fold difference in turning rate between the best and worst performers. Hyperextension of the margin occurred only at activation wave speeds near the material wave speed, suggesting resonance. This hyperextension resulted in a 34-fold asymmetry in the circulation of the vortex ring between the inside and outside of the turn. Experimental recording of the activation speed confirmed that jellyfish actuate within this range, and flow visualization using particle image velocimetry validated the corresponding fluid dynamics of the numerical model. This suggests that neuromechanical wave resonance plays an important role in the robustness of an organism's locomotory system and presents an undiscovered constraint on the evolution of flexible organisms. Understanding these dynamics is essential for developing actuators in soft body robotics and bioengineered pumps.

Lift and Drag Acting on the Shell of the American Horseshoe Crab (Limulus polyphemus).

The intertidal zone is a turbulent landscape where organisms face numerous mechanical challenges from powerful waves. A model for understanding the solutions to these physical problems, the American horseshoe crab (Limulus polyphemus), is a marine arthropod that mates in the intertidal zone, where it must contend with strong ambient flows to maintain its orientation during locomotion and reproduction. Possible strategies to maintain position include either negative lift generation or the minimization of positive lift in flow. To quantify flow over the shell and the forces generated, we laser-scanned the 3D shape of a horseshoe crab, and the resulting digital reconstruction was used to 3D-print a physical model. We then recorded the movement of tracking particles around the shell model with high-speed video and analyzed the time-lapse series using particle image velocimetry (PIV). The velocity vector fields from PIV were used to validate numerical simulations performed with the immersed boundary (IB) method. IB simulations allowed us to resolve the forces acting on the shell, as well as the local three-dimensional flow velocities and pressures. Both IB simulations and PIV analysis of vorticity and velocity at a flow speed of 13 cm/s show negative lift for negative and zero angles of attack, and positive lift for positive angles of attack in a free-stream environment. In shear flow simulations, we found near-zero lift for all orientations tested. Because horseshoe crabs are likely to be found primarily at near-zero angles of attack, we suggest that this negative lift helps maintain the orientation of the crab during locomotion and mating. This study provides a preliminary foundation for assessing the relationship between documented morphological variation and potential environmental variation for distinct populations of horseshoe crabs along the Atlantic Coast. It also motivates future studies which could consider the stability of the horseshoe crab in unsteady, oscillating flows.