Navigation of C. elegans in three-dimensional media: roll maneuvers 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 in vestigations 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.