Swimming behavior of cryptophyte prey affects prey preference of the ambush-feeding ciliate Mesodinium rubrum

Abstract

The mixotrophic ciliate Mesodinium rubrum is an ambush feeder relying on cryptophyte prey motility for prey encounter and perception; therefore, cryptophyte species-specific swimming behaviors affect M. rubrum’s prey preference. Here, a high-speed microscale imaging system was used to quantify the swimming behaviors of 3 cryptophyte species (Teleaulax amphioxeia, Storeatula major, and Guillardia theta) and to conduct quantitative microvideography of M. rubrum-T. amphioxeia predator-prey interaction. T. amphioxeia, a preferred prey of M. rubrum, swam at path-averaged speeds of 155 ± 73 µm s-1 along rather straight paths. In contrast, S. major regularly tumbled slowly downward or upward at 64 ± 16 µm s-1, while G. theta moved slowly in looped/curved trajectories at 57 ± 15 µm s-1; neither supports M. rubrum growth. Only while motionlessly sinking passively did M. rubrum detect and initiate an attack on swimming T. amphioxeia at reaction distances of 8.2 ± 8.2 µm. It seemed that M. rubrum needed to use oral tentacles to initially poke T. amphioxeia’s ventral posterior part and subsequently poke the prey multiple times in a short duration to compromise the prey’s escape ability, presumably by discharging extrusomes into the prey. T. amphioxeia also responded to nearby predators by switching to tumbling similar to S. major in normal swimming, suggesting an effective anti-predator defense behavior that prevents M. rubrum from accurately poking the prey’s ventral posterior part. T. amphioxeia swimming at significantly higher speeds leads to sufficiently high prey encounters and hydrodynamic signals for M. rubrum, thereby partially explaining M. rubrum’s ability to select T. amphioxeia prey.