Hydrodynamics of small marine organisms: A mechanistic exploration of traits and trade-offs for flagellates and filter feeders

Abstract

Although typically not visible to the naked eye, planktonic organisms play key roles for the functioning of the aquatic ecosystem. They display a huge morphological and functional diversity ranging from microscopic bacteria to meter-sized gelatinous organisms. Due to their intimate interaction with the water as habitat and medium, flows are essential to the survival strategies of plankton. Many, even unicellular, species are motile and create various kinds of flows that accompany swimming and can be used for prey and nutrient collection. On the other hand, the flow disturbances due to prey organisms can also be used by predators for remote detection via FLow-sensing. In this study we use mechanistic models to explore and quantify the traits and trade-offs that relate to the swimming, feeding, and predator avoidance in small marine organisms. Unicellular flagellates create flows with whip-like appendages that in different species can have various numbers, lengths, and beat patterns. We use an analytical hydrodynamics model to distinguish those characteristics. We represent the cell body as a solid sphere and the action of each flagellum by a point force on the water that creates a flow and propels the organism. The different swimming modes are quantied by the number, magnitude, position, and direction of the point forces in the model, which lead to specific flow patterns and kinematics. We use the model to represent two biflagellated haptophyte species that both have a left-right symmetric flagellar arrangement, but different lengths and beat patterns. The time-resolved near-cell flows that are measured with micro particle image velocimetry can be well represented by the analytical model and allow us to assign characteristic average force positions to the two species. By calculating swimming speed, size of the disturbance zone, and advective prey encounter rates for different force positions, we find that equatorial arrangements are favoured for fast and stealthy swimming, while puller swimmers with front arrangements exhibit increased prey encounter rates. We present further possibilities of the model to evaluate the swimming speed due to different forces during a periodic swimming stroke and to calculate characteristics of the helical trajectory for asymmetric swimmers. A second group of organisms that we investigate are filter feeders that use fibrous filter structures to collect and sieve prey from the dilute suspension that ocean water represents. We closely investigate microbial filter feeding on the example of choanoflagellates, which are unicellular organisms that use a single flagellum to drive a feeding flow through a collar filter. The volume flow rates of individuals measured with micro particle tracking velocimetry by far exceeded numerically simulated and analytically estimated maximum flow rates based on the observed flagellum kinematics. This discrepancy and previous findings of so-called flagellar vanes in related species lead us to suggest such a structure in several choanoflagellate species, which can increase the driving force of the flagellar beat and can account for the large measured flow rates as we indicate with computational fluid dynamics and analytical calculations. We further consider a trade-off which leads to optimum filter spacings for maximum prey encounter. The flagellar driving force can create large flow rates through a coarse mesh due to low resistance. On the other hand, a fine mesh can retain a larger range of prey sizes from the suspension. Another theme is the emergence of large gelatinous body plans among planktonic filter feeders. Gelatinous organisms are characterised by a much more watery body composition than the typical cell. In order to understand and quantify the general trade-offs for filter feeders with different body plans we developed an energy budget model. The model accounts for energy intake from prey collection and energy expenditure from active flow creation as well as basal respiration. The prey clearance rates of filter feeders are found to be limited by the maximum force that their biological motor can create. The filter area per body biomass needs to be large to prevent starvation. Thus a simple, but wide-ranging result of the model is that larger organisms (with a large biomass) have a stronger need than microbes to increase their area and they do this by becoming gelatinous. As a last study of this project we explore the effect of prey size on prey capture rates by organisms, which encounter their prey directly on the cell surface. We numerically calculate the advective-diffusive capture of finite-sized prey on a spherical cell in a simple Stokes flow. We find high capture rates both for the smallest and the largest prey, and we identify a minimum of the capture rate for intermediate prey. We rationalise and explain the observed trends in an analytical model for the capture of finite-sized prey. We additionally investigate "sloppy" feeders, which exhibit severe prey losses when the predator-prey contact time is short. Sloppy feeders mainly lose small diffusive particles, such that they predominantly capture the largest prey.