Digital holographic microscopy reveals prey-induced changes in swimming behavior of predatory dinoflagellates

Abstract

The shallow depth of field of conventional microscopy hampers analyses of 3D swimming behavior of fast dinoflagellates, whose motility influences macroassemblages of these cells into often-observed dense “blooms.” The present analysis of cinematic digital holographic microscopy data enables simultaneous tracking and characterization of swimming of thousands of cells within dense suspensions. We focus on Karlodinium veneficum and Pfiesteria piscicida, mixotrophic and heterotrophic dinoflagellates, respectively, and their preys. Nearest-neighbor distance analysis shows that predator and prey cells are randomly distributed relative to themselves, but, in mixed culture, each predator clusters around its respective prey. Both dinoflagellate species exhibit complex highly variable swimming behavior as characterized by radius and pitch of helical swimming trajectories and by translational and angular velocity. K. veneficum moves in both left- and right-hand helices, whereas P. piscicida swims only in right-hand helices. When presented with its prey (Storeatula major), the slower K. veneficum reduces its velocity, radius, and pitch but increases its angular velocity, changes that reduce its hydrodynamic signature while still scanning its environment as “a spinning antenna.” Conversely, the faster P. piscicida increases its speed, radius, and angular velocity but slightly reduces its pitch when exposed to prey (Rhodomonas sp.), suggesting the preferred predation tactics of an “active hunter.”