Alejandro Bilbao

Nematode locomotion in unconfined and confined fluids

The millimeter-long soil-dwelling nematode Caenorhabditis elegans propels itself by producing undulations that propagate along its body and turns by assuming highly curved shapes. According to our recent study [V. Padmanabhan et al., PLoS ONE 7, e40121 (2012)10.1371/journal.pone.0040121] all these postures can be accurately described by a piecewise-harmonic-curvature model. We combine this curvature-based description with highly accurate hydrodynamic bead models to evaluate the normalized velocity and turning angles for a worm swimming in an unconfined fluid and in a parallel-wall cell. We find that the worm moves twice as fast and navigates more effectively under a strong confinement, due to the large transverse-to-longitudinal resistance-coefficient ratio resulting from the wall-mediated far-field hydrodynamic coupling between body segments. We also note that the optimal swimming gait is similar to the gait observed for nematodes swimming in high-viscosity fluids. Our bead models allow us to determine t...

Roll maneuvers are essential for active reorientation of Caenorhabditis elegans in 3D media

Significance Investigations of the free-living nematode Caenorhabditis elegans give powerful insights into fundamental biological processes that are conserved across species. Locomotion of this model organism is used to assess muscular and neural defects and score impacts of genetic mutations and pharmacological interventions. Existing analyses of the nematode gait have been focused on 2D locomotion, and 3D motion remains largely unexplored. We identify and mathematically describe a unique 3D behavioral pattern in burrowing and swimming—a roll maneuver—which, in combination with 2D turns, allows the nematode to explore bulk media. Our results provide important insights into 3D neuromuscular actuation and may be used to develop better assays for locomotion phenotype analysis. Locomotion of the nematode Caenorhabditis elegans is a key observable used in investigations ranging from behavior to neuroscience to aging. However, while the natural environment of this model organism is 3D, quantitative investigations of its locomotion have been mostly limited to 2D motion. Here, we present a quantitative analysis of how the nematode reorients itself in 3D media. We identify a unique behavioral state of C. elegans—a roll maneuver—which is an essential component of 3D locomotion in burrowing and swimming. The rolls, associated with nonzero torsion of the nematode body, result in rotation of the plane of dorsoventral body undulations about the symmetry axis of the trajectory. When combined with planar turns in a new undulation plane, the rolls allow the nematode to reorient its body in any direction, thus enabling complete exploration of 3D space. The rolls observed in swimming are much faster than the ones in burrowing; we show that this difference stems from a purely hydrodynamic enhancement mechanism and not from a gait change or an increase in the body torsion. This result demonstrates that hydrodynamic viscous forces can enhance 3D reorientation in undulatory locomotion, in contrast to known hydrodynamic hindrance of both forward motion and planar turns.Free-living nematode Caenorhabditis elegans is a powerful genetic model, essential for investigations ranging from behavior to neuroscience to aging, and locomotion is a key observable used in these studies. However, despite the fact that in its natural environment C. elegans moves in three-dimensional (3D) complex media (decomposing organic matter and water), quantitative investigations of its locomotion have been limited to two-dimensional (2D) motion. Based on our recent quantitative analysis of 2D turning maneuvers [Phys. Fluids 25, 081902 (2013)] we follow with the first quantitative description of how C. elegans moves in 3D environments. We show that by superposing body torsion and 2D undulations, a burrowing or swimming nematode can rotate the undulation plane. A combination of these roll maneuvers and 2D turns associated with variation of undulation-wave parameters allows the nematode to explore 3D space. We apply our model to analyze 3D chemotaxis of nematodes burrowing in a gel and swimming in water; we conclude that the nematode can achieve efficient chemotaxis in different environments without adjusting its sensory-motor response to chemical signals. Implications of our findings for understanding of 3D neuromuscular control of nematode body are discussed.