Emergent Collective Locomotion in an Active Polymer Model of Entangled Worm Blobs

Abstract

Numerous worm and arthropod species form physically-connected aggregations in which interactions among individuals give rise to emergent macroscale dynamics and functionalities that enhance collective survival. In particular, some aquatic worms such as the California blackworm (Lumbriculus variegatus) entangle their bodies into dense blobs to shield themselves against external stressors and preserve moisture in dry conditions. Motivated by recent experiments revealing emergent locomotion in blackworm blobs, we investigate the collective worm dynamics by modeling each worm as a self-propelled Brownian polymer. Though our model is two-dimensional, compared to real three-dimensional worm blobs, we demonstrate how a simulated blob can collectively traverse temperature gradients via the coupling between the active motion and the environment. By performing a systematic parameter sweep over the strength of attractive forces between worms, and the magnitude of their directed self-propulsion, we obtain a rich phase diagram which reveals that effective collective locomotion emerges as a result of finely balancing a tradeoff between these two parameters. Our model brings the physics of active filaments into a new meso- and macroscale context and invites further theoretical investigation into the collective behavior of long, slender, semi-flexible organisms.

Amorphous entangled active matter

“…10,19 Less is known about how structural properties evolve as particle shape evolves, despite such transitions existing in nature (as in ant systems, in cytoskeleton and f-actin, in polymer rheology, and in aquatic worm blobs). 4,[27][28][29][30][31][32][33][34] In this work, we focus on an active matter system composed of shape-changing particles, where as we demonstrate below, rich and non-intuitive material physics can be uncovered. How macroscopic material properties are affected by the microscopic movements of its constituents is under-studied.…”

“…We compare some of these properties to biological experiment using California blackworms (Lumbriculus variegatus), whose collectives demonstrate a non-trivial macroscopic rheological analogue with features and properties from microscopic entanglement. 4,32,42 2 Materials and methods…”

Oxygenation-Controlled Collective Dynamics in Aquatic Worm Blobs

“…These worms can form a highly compact and dense worm "blob" (Fig. 1b) structure that exhibits properties comparable to a highly viscous non-Newtonian fluid when outside of granular substrate or detritus (Deblais et al 2020a,b;Nguyen et al 2021;Ozkan-Aydin et al 2021). As with most oligochaetes, this agglomeration is due to their thigmotactic behavior, which causes them to wrap around and tangle with each other for survival against desiccation, predation, and other factors (Timm and Martin 2015;Zirbes et al 2010).…”

Amorphous Entangled Active Matter

“…In granular media for example, there has been some research in the evolution of the macroscopic state dynamics. Most research was performed with external loading 10,19 ; however, less is known about how structural properties evolve as particle shape evolves, despite such transitions existing in nature (as in ant systems, in cytoskeleton and f-actin, in polymer rheology, and in aquatic worm blobs) 4,[27][28][29][30][31][32][33][34] . In this work, we focus on an active matter system composed of shape-changing particles, where as we demonstrate below, rich and non-intuitive material physics can be uncovered.…”

“…Using stress-strain tests on an entangled chain of smarticles, we discover various properties related to their emergent auxeticity. Finally, we compare a few of these properties to biological experiment using California blackworms (Lumbriculus variegatus), whose collectives demonstrate a non-trivial macroscopic rheological analogue with features and properties from microscopic entanglement 4,32,42 .…”