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. 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.
Early root growth is critical for plant establishment and survival. We have identified a molecular pathway required for helical root tip movement known as circumnutation. Here, we report a multiscale investigation of the regulation and function of this phenomenon. We identify key cell signaling events comprising interaction of the ethylene, cytokinin, and auxin hormone signaling pathways. We identify the gene Oryza sativa histidine kinase-1 (HK1) as well as the auxin influx carrier gene OsAUX1 as essential regulators of this process in rice. Robophysical modeling and growth challenge experiments indicate circumnutation is critical for seedling establishment in rocky soil, consistent with the long-standing hypothesis that root circumnutation facilitates growth past obstacles. Thus, the integration of robotics, physics, and biology has elucidated the functional importance of root circumnutation and uncovered the molecular mechanisms underlying its regulation. Significance Root growth in soil is complex. With limited sensory input, roots must navigate an environment containing heterogeneities such as rocks and compaction. The ability of roots to penetrate soil is crucial for water and nutrient uptake as well as mechanical anchorage. Here, we describe a molecular framework controlling helical root growth known as circumnutation. Functional characterization of circumnutation is consistent with the hypothesis that it is crucial for exploratory behavior and substrate penetration. This work lays a foundation for an integrated understanding of how roots grow in soil.
Earthworms can move beneath soil by expanding parts of their bodies radially; bristles called setae work as anchors during surface locomotion but their efficacy during subsurface movement is unknown. We designed a soft, wormlike robot which models the putative earthworm anchoring mechanisms by combining Kirigami skin with radially-expanding pneumatic actuators. The robot consists of three pneumatic actuator segments: head and tail segments that expand radially as anchors, and a middle segment that elongates the body. The Kirigami structure pops up when an actuator is radially expanded, forming bristle-like spikes which are perpendicular to surface, and folds back down when deflated, forming a smoother skin structure. The robustness of Kirigami skin is improved by introducing a novel silicone-plastic layer fabrication method. The pop-up features penetrate the soil without significantly deforming the soil surface, improving the anchoring ability of the segment. Improvements in anchoring are studied systematically by measuring the differences in segment drag forces beneath soil. The performance of robot locomotion in soil terrain with or without Kirigami skin was measured in several terrain conditions (within a cohesive garden soil channel, buried in cohesive soil) as the robot dragged payloads behind it. The Kirigami skin-covered robot exhibits a greater maximum drag force (improved from 2.1±0.3 N to 5.5±0.5 N in 25mm hole diameter condition), greater forward displacement, and higher traction (e.g., with an 40g payload, the 3.7±2.8 cm improved to a 12.5±0. 1cm in 6 gait cycles).