Multipolar Capillary Interactions and Self-Assembly of Plant Bioparticles on Fluid Interfaces*

Marchantia polymorpha, or common liverworts, reproduce asexually by growing cup-like structures on their leafy thalli which contain multicellular propagules called gemmae. When rain fills the gemmae cups, mature gemmae are released, adsorb to the air-water interface, and subsequently are splashed out to grow into new plants. Gemmae have long been assumed to be passive agents, but their capillary interactions while attached to the air-water interface suggest they play a much more active role in liverwort reproduction. To investigate this, we directly measure capillary interactions of gemmae on both flat and curved fluid interfaces using brightfield microscopy and optical profilometry, and find that gemmae adsorbed to the water surface interact and self-assemble as capillary multipoles. We analyze fluid surface profiles around individual and pairs of gemmae and find that the capillary multipole character is dominantly quadrupolar. We also simulate this system using finite element methods to numerically calculate energetically optimal assembly configurations. Intriguingly, we observe different assembly behavior of multiple gemmae on flat fluid interfaces versus in their natural environment. This suggests that the gemmae cups may have evolved to shape the water surface to arrange the gemmae for better splash dispersal.