Seeking safety: Movement dynamics after post-contact immobility.

Post-contact immobility (PCI) is a final attempt to avoid predation. Here, for the first time, we examine the pattern of movement and immobility when antlion larvae resume activity after PCI. To simulate contact with, and escape from, a predator we dropped the larvae onto three different substrates: Paper, Shallow sand (2.3mm-deep) and Deep sand (4.6mm-deep). The Paper lining a Petri dish represented a hard surface that antlion larvae could not penetrate to hide. The Shallow sand permitted the antlions to dig but not to submerge completely whereas the Deep sand allowed them both to dig and to submerge. We tracked their paths automatically and recorded alternating immobility and movement durations over 90min. On the impenetrable substrate, antlion larvae showed super-diffusive dispersal, their movement durations became longer, their immobility durations became shorter and their instantaneous speeds increased. This is consistent with the antlions needing to leave an area of hard substrate and quickly to find somewhere to hide. On Shallow sand, antlion larvae exhibited a modest increase in movement duration, a modest decrease in immobility duration and a concomitant diffusive dispersal. This is consistent with their use of a spiral search, presumably for a suitable depth of sand, to conceal themselves. On Deep sand, the movement and immobility durations of the antlion larvae did not change and their dispersal was sub-diffusive because they were able to bury themselves. On Paper, the distribution of immobility durations had a long tail, consistent with a log-normal distribution. On Shallow and Deep sand, most of the distribution was fitted better by a power law or a log-normal. Our results suggest that PCI in antlion larvae is a disruptive event and that post-PCI movement and immobility gradually return to the pattern typical of intermittent locomotion, depending on the scope for burying and hiding in the substrate.

How do cicadas emerge together? Thermophysical aspects of their collective decision-making.

Periodical cicadas exhibit life cycles with durations of 13 or 17 years, and it is now accepted that large prime cycles arose to avoid synchrony with predators. Less well explored is how, in the face of intrinsic biological and environmental noise, insects within a brood emerge together in large successive swarms from underground during springtime warming. Here, we consider the decision-making process of underground cicadas experiencing random, spatially correlated thermal microclimates such as those in nature. Introducing short-range communication between insects leads to an Ising model of consensus building with a quenched, spatially correlated random magnetic field and annealed site dilution, which displays the kinds of collective swarms seen in nature. These results highlight the need for fieldwork to quantify the spatial fluctuations in thermal microclimates and their relationship to the spatiotemporal dynamics of swarm emergence.

Swimming, Feeding, and Inversion of Multicellular Choanoflagellate Sheets.

The recent discovery of the striking sheetlike multicellular choanoflagellate species Choanoeca flexa that dynamically interconverts between two hemispherical forms of opposite orientation raises fundamental questions in cell and evolutionary biology, as choanoflagellates are the closest living relatives of animals. It similarly motivates questions in fluid and solid mechanics concerning the differential swimming speeds in the two states and the mechanism of curvature inversion triggered by changes in the geometry of microvilli emanating from each cell. Here we develop fluid dynamical and mechanical models to address these observations and show that they capture the main features of the swimming, feeding, and inversion of C. flexa colonies, which can be viewed as active, shape-shifting polymerized membranes.

Phototaxis of Chlamydomonas arises from a tuned adaptive photoresponse shared with multicellular Volvocine green algae.

A fundamental issue in biology is the nature of evolutionary transitions from unicellular to multicellular organisms. Volvocine algae are models for this transition, as they span from the unicellular biflagellate Chlamydomonas to multicellular species of Volvox with up to 50,000 Chlamydomonas-like cells on the surface of a spherical extracellular matrix. The mechanism of phototaxis in these species is of particular interest since they lack a nervous system and intercellular connections; steering is a consequence of the response of individual cells to light. Studies of Volvox and Gonium, a 16-cell organism with a plate-like structure, have shown that the flagellar response to changing illumination of the cellular photosensor is adaptive, with a recovery time tuned to the rotation period of the colony around its primary axis. Here, combining high-resolution studies of the flagellar photoresponse of micropipette-held Chlamydomonas with 3D tracking of freely swimming cells, we show that such tuning also underlies its phototaxis. A mathematical model is developed based on the rotations around an axis perpendicular to the flagellar beat plane that occur through the adaptive response to oscillating light levels as the organism spins. Exploiting a separation of timescales between the flagellar photoresponse and phototurning, we develop an equation of motion that accurately describes the observed photoalignment. In showing that the adaptive timescales in Volvocine algae are tuned to the organisms' rotational periods across three orders of magnitude in cell number, our results suggest a unified picture of phototaxis in green algae in which the asymmetry in torques that produce phototurns arise from the individual flagella of Chlamydomonas, the flagellated edges of Gonium, and the flagellated hemispheres of Volvox.

Collapse of a hemicatenoid bounded by a solid wall: instability and dynamics driven by surface Plateau border friction.

The collapse of a catenoidal soap film when the rings supporting it are moved beyond a critical separation is a classic problem in interface motion in which there is a balance between surface tension and the inertia of the surrounding air, with film viscosity playing only a minor role. Recently [Goldstein et al., Phys. Rev. E, 2021, 104, 035105], we introduced a variant of this problem in which the catenoid is bisected by a glass plate located in a plane of symmetry perpendicular to the rings, producing two identical hemicatenoids, each with a surface Plateau border (SPB) on the glass plate. Beyond the critical ring separation, the hemicatenoids collapse in a manner qualitatively similar to the bulk problem, but their motion is governed by the frictional forces arising from viscous dissipation in the SPBs. We present numerical studies of a model that includes classical laws in which the frictional force fv for SPB motion on wet surfaces is of the form fv ∼ Can, where Ca is the capillary number. Our experimental data on the temporal evolution of this process confirms the expected value n = 2/3 for mobile surfactants and stress-free interfaces. This study can help explain the fragmentation of bubbles inside very confined geometries such as porous materials or microfluidic devices.

Biofilm Growth under Elastic Confinement.

Bacteria often form surface-bound communities, embedded in a self-produced extracellular matrix, called biofilms. Quantitative studies of bioflim growth have typically focused on unconfined expansion above solid or semisolid surfaces, leading to exponential radial growth. This geometry does not accurately reflect the natural or biomedical contexts in which biofilms grow in confined spaces. Here, we consider one of the simplest confined geometries: a biofilm growing laterally in the space between a solid surface and an overlying elastic sheet. A poroelastic framework is utilized to derive the radial growth rate of the biofilm; it reveals an additional self-similar expansion regime, governed by the Poisson's ratio of the matrix, leading to a finite maximum radius, consistent with our experimental observations of growing Bacillus subtilis biofilms confined by polydimethylsiloxane.

Cellular organization in lab-evolved and extant multicellular species obeys a maximum entropy law.

The prevalence of multicellular organisms is due in part to their ability to form complex structures. How cells pack in these structures is a fundamental biophysical issue, underlying their functional properties. However, much remains unknown about how cell packing geometries arise, and how they are affected by random noise during growth - especially absent developmental programs. Here, we quantify the statistics of cellular neighborhoods of two different multicellular eukaryotes: lab-evolved 'snowflake' yeast and the green alga Volvox carteri. We find that despite large differences in cellular organization, the free space associated with individual cells in both organisms closely fits a modified gamma distribution, consistent with maximum entropy predictions originally developed for granular materials. This 'entropic' cellular packing ensures a degree of predictability despite noise, facilitating parent-offspring fidelity even in the absence of developmental regulation. Together with simulations of diverse growth morphologies, these results suggest that gamma-distributed cell neighborhood sizes are a general feature of multicellularity, arising from conserved statistics of cellular packing.

Fluid Mechanics of Mosaic Ciliated Tissues.

In tissues as diverse as amphibian skin and the human airway, the cilia that propel fluid are grouped in sparsely distributed multiciliated cells (MCCs). We investigate fluid transport in this "mosaic" architecture, with emphasis on the trade-offs that may have been responsible for its evolutionary selection. Live imaging of MCCs in embryos of the frog Xenopus laevis shows that cilia bundles behave as active vortices that produce a flow field accurately represented by a local force applied to the fluid. A coarse-grained model that self-consistently couples bundles to the ambient flow reveals that hydrodynamic interactions between MCCs limit their rate of work so that they best shear the tissue at a finite but low area coverage, a result that mirrors findings for other sparse distributions such as cell receptors and leaf stomata.

Geometry of catenoidal soap film collapse induced by boundary deformation.

Experimental and theoretical work reported here on the collapse of catenoidal soap films of various viscosities reveal the existence of a robust geometric feature that appears not to have been analyzed previously; prior to the ultimate pinchoff event on the central axis, which is associated with the formation of a well-studied local double-cone structure folded back on itself, the film transiently consists of two acute-angle cones connected to the supporting rings, joined by a central quasicylindrical region. As the cylindrical region becomes unstable and pinches, the opening angle of those cones is found to be universal, independent of film viscosity. Moreover, that same opening angle at pinching is found when the transition occurs in a hemicatenoid bounded by a surface. The approach to the conical structure is found to obey classical Keller-Miksis scaling of the minimum radius as a function of time, down to very small but finite radii. While there is a large body of work on the detailed structure of the singularities associated with ultimate pinchoff events, these large-scale features have not been addressed. Here we study these geometrical aspects of film collapse by several distinct approaches, including a systematic analysis of the linear and weakly nonlinear dynamics in the neighborhood of the saddle node bifurcation leading to collapse, both within mean curvature flow and the physically realistic Euler flow associated with the incompressible dynamics of the surrounding air. These analyses are used to show how much of the geometry of collapsing catenoids is accurately captured by a few active modes triggered by boundary deformation. A separate analysis based on a mathematical sequence of shapes progressing from the critical catenoid towards the Goldschmidt solution is shown to predict accurately the cone angle at pinching. We suggest that the approach to the conical structures can be viewed as passage close to an unstable fixed point of conical similarity solutions. The overall analysis provides the basis for the systematic study of more complex problems of surface instabilities triggered by deformations of the supporting boundaries.

An "occlusive thrombosis-on-a-chip" microfluidic device for investigating the effect of anti-thrombotic drugs.

Cardiovascular disease remains one of the world's leading causes of death. Myocardial infarction (heart attack) is triggered by occlusion of coronary arteries by platelet-rich thrombi (clots). The development of new anti-platelet drugs to prevent myocardial infarction continues to be an active area of research and is dependent on accurately modelling the process of clot formation. Occlusive thrombi can be generated in vivo in a range of species, but these models are limited by variability and lack of relevance to human disease. Although in vitro models using human blood can overcome species-specific differences and improve translatability, many models do not generate occlusive thrombi. In those models that do achieve occlusion, time to occlusion is difficult to measure in an unbiased and objective manner. In this study we developed a simple and robust approach to determine occlusion time of a novel in vitro microfluidic assay. This highlighted the potential for occlusion to occur in thrombosis microfluidic devices through off-site coagulation, obscuring the effect of anti-platelet drugs. We therefore designed a novel occlusive thrombosis-on-a-chip microfluidic device that reliably generates occlusive thrombi at arterial shear rates by quenching downstream coagulation. We further validated our device and methods by using the approved anti-platelet drug, eptifibatide, recording a significant difference in the "time to occlude" in treated devices compared to control conditions. These results demonstrate that this device can be used to monitor the effect of antithrombotic drugs on time to occlude, and, for the first time, delivers this essential data in an unbiased and objective manner.