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Edited by John A. Rogers, Northwestern University, Evanston, IL, and approved December 31, 2020 (received for review May 27, 2020)
Significance
Living organisms form collectives across all scales, enabling biological functions not accessible by individuals alone. In a few cases, the individuals are physically connected to each other, forming an additional class of entangled active matter systems with emergent mechanofunctionalities of the collective. Here, we describe the dynamics of macroscopic aquatic worms that braid their long, soft bodies to form large entangled worm blobs. We discover that the worm blob behaves as a living material to undergo dynamic shape transformations to reduce evaporation or break-symmetry and locomote to safety against thermal stresses. We validate our biological hypotheses in robophysical swarming blobs, which pave the way for additional classes of mechanofunctional active matter systems and collective emergent robotics.
Abstract
Living systems at all scales aggregate in large numbers for a variety of functions including mating, predation, and survival. The majority of such systems consist of unconnected individuals that collectively flock, school, or swarm. However, some aggregations involve physically entangled individuals, which can confer emergent mechanofunctional material properties to the collective. Here, we study in laboratory experiments and rationalize in theoretical and robophysical models the dynamics of physically entangled and motile self-assemblies of 1-cm-long California blackworms (Lumbriculus variegatus, Annelida: Clitellata: Lumbriculidae). Thousands of individual worms form braids with their long, slender, and flexible bodies to make a three-dimensional, soft, and shape-shifting “blob.” The blob behaves as a living material capable of mitigating damage and assault from environmental stresses through dynamic shape transformations, including minimizing surface area for survival against desiccation and enabling transport (negative thermotaxis) from hazardous environments (like heat). We specifically focus on the locomotion of the blob to understand how an amorphous entangled ball of worms can break symmetry to move across a substrate. We hypothesize that the collective blob displays rudimentary differentiation of function across itself, which when combined with entanglement dynamics facilitates directed persistent blob locomotion. To test this, we develop a robophysical model of the worm blobs, which displays emergent locomotion in the collective without sophisticated control or programming of any individual robot. The emergent dynamics of the living functional blob and robophysical model can inform the design of additional classes of adaptive mechanofunctional living materials and emergent robotics.
Footnotes
- ↵1To whom correspondence may be addressed. Email: saadb{at}chbe.gatech.edu.
Author contributions: Y.O.-A., D.I.G., and M.S.B. designed research; Y.O.-A. conceived the setups and performed animal and robot experiments; Y.O.-A. derived the model and analyzed data; and Y.O.-A., D.I.G., and M.S.B. wrote the paper.
The authors declare no competing interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2010542118/-/DCSupplemental.
Data Availability.
All study data are included in this article and/or SI Appendix.
Published under the PNAS license.
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Collective dynamics in entangled worm and robot blobs
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- Physical Sciences
- Engineering
- Biological Sciences
- Physiology
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