Foraging trade-offs,flagellar arrangements,and flow architecture of planktonic protists

Unicellular flagellated protists are a key element in aquatic microbial food webs. They all use flagella to swim and to generate feeding currents to encounter prey and enhance nutrient uptake. At the same time, the beating flagella create flow disturbances that attract flow-sensing predators. Protists have highly diverse flagellar arrangements in terms of number of flagella and their position, beat pattern, and kinematics, but it is unclear how the various arrangements optimize the fundamental trade-off between resource acquisition and predation risk. Here we describe the near-cell flow fields produced by 15 species and demonstrate consistent relationships between flagellar arrangement and swimming speed and between flagellar arrangement and flow architecture, and a trade-off between resource acquisition and predation risk. The flow fields fall in categories that are qualitatively described by simple point force models that include the drag force of the moving cell body and the propulsive forces of the flagella. The trade-off between resource acquisition and predation risk varies characteristically between flow architectures: Flagellates with multiple flagella have higher predation risk relative to their clearance rate compared to species with only one active flagellum, with the exception of the highly successful dinoflagellates that have simultaneously achieved high clearance rates and stealth behavior due to a unique flagellar arrangement. Microbial communities are shaped by trade-offs and environmental constraints, and a mechanistic explanation of foraging trade-offs is a vital part of understanding the eukaryotic communities that form the basis of pelagic food webs.

Unicellular flagellated protists play a key role in the biogeochemical cycles of the global ocean. Their photosynthetic activity and grazing on microbes are major processes in the microbial food web, and they may control the populations of bacteria and cyanobacteria (1). By being grazed, they transfer primary production to higher trophic levels (2–4). Thus, flagellates are both consumers and prey, but we do not understand how their resource acquisition trades off against predation mortality, or how this trade-off shapes their foraging behavior.In the low Reynolds number (Re) world of protists, viscosity impedes predator-prey contact. The physical mechanisms that nevertheless allow flagellates to daily clear a volume of water for prey that corresponds to approximately 10⁶ times their own cell volume (5, 6) are not well understood. Many marine flagellates are mixotrophic and can acquire resources both through photosynthesis and by eating other organisms (7). Their demand for inorganic mineral nutrients is also constrained by viscosity that retards the advective enhancement of diffusive uptake (8).To encounter prey and enhance advective transport of nutrients, protists may swim or create a feeding current through the beating of one or several flagella (9, 10). However, the beating of flagella produces fluid disturbances that exposes the flagellate to its rheotactic (flow-sensing) predators (11). Small flagellates are grazed by microzooplankton, many of which perceive their prey from the fluid disturbance that the prey generates (12, 13). Thus, there are fundamental foraging trade-offs. Such trade-offs are largely unexplored among the eukaryotic microbes that form the basis of aquatic food webs. This is crucial, because the diversity of microbial communities is determined by such trade-offs in concert with environmental constraints (14–17). Microbial diversity in turn governs the functionality and “services” of microbial communities, and hence also their role in ocean biogeochemistry (18, 19).Here we explore the trade-off between resource acquisition and predation risk in marine nanoflagellates and microflagellates by describing the flow fields produced by the action of their flagella. The quantification of near-cell feeding currents has been reported in only a few species of free-swimming protists (10, 20). The kinematics, wave patterns, and arrangement and number of flagella are highly diverse among flagellated protists (Fig. 1). Theoretical models suggest that the feeding currents and fluid signal generated by a swimming cell depends on the arrangement of the flagella (11, 13, 21, 22). We use microparticle image velocimetry (µPIV) to visualize and quantify the flow fields generated by free-swimming planktonic protists with diverse flagellar arrangements and beat patterns. We show how the different modes of swimming produce very different flow architectures and demonstrate a trade-off between resource acquisition and predation risk in flagellated protists.Open in a separate windowFig. 1.Schematic overview of the diverse flagellar arrangements and beat patterns represented in this study. Latin names below each taxonomic group indicate the species (or other taxonomic unit) examined. Flagellar hairs are drawn when feasible, but some flagellar morphologies (e.g., the dinoflagellates) are deliberately simplified (25, 63). Redrawn from several sources; not to scale.