Mechanisms and fluid dynamics of foraging in heterotrophic nanoflagellates

Abstract

Heterotrophic nanoflagellates are the main consumers of bacteria and picophytoplankton in the ocean. In their microscale world, viscosity impedes predator–prey contact, and the mechanisms that allow flagellates to daily clear a volume of water for prey corresponding to 106 times their own volume is unclear. It is also unclear what limits observed maximum ingestion rates of about 104 bacterial preys per day. We used high‐speed video microscopy to describe feeding flows, flagellum kinematics, and prey searching, capture, and handling in four species with different foraging strategies. In three species, prey handling times limit ingestion rates and account well for their reported maximum values. Similarly, observed feeding flows match reported clearance rates. Simple point force models allowed us to estimate the forces required to generate the feeding flows, between 4 and 13 pN, and consistent with the force produced by the hairy (hispid) flagellum, as estimated using resistive force theory. Hispid flagella can produce a force that is much higher than the force produced by a naked (smooth) flagellum with similar kinematics, and the hairy flagellum is therefore key to foraging in most nanoflagellates. Our findings provide a mechanistic underpinning of observed functional responses of prey ingestion rates in nanoflagellates.

Hydrodynamic interactions are key in thrust-generation of hairy flagella

“…3(a)]. We calculate the time-averaged thrust, Fy = 6.8 pN, consistent with estimates based on the observed flow in tethered individuals [21]. Furthermore, the flow field shows that there is a relatively weak upward flow in the middle of the region swept by the hairy flagellum, and a stronger downward flow on the sides.…”

“…For a quantitative comparison with resistive force theory (RFT), we consider the time-averaged drag-based thrust generated by a single hair, which in RFT is [21,26,27]…”

“…The presence of hairs on the flagellum is key to foraging in flagellates. Not only does the reversal of the flow increase the capture efficiency of prey arriving in the feeding current [21], but the hairs also increase the thrust generation significantly as compared to a smooth flagellum with the same beat kinematics or the same power expenditure. For a comparison of the efficiency of the thrust generation by naked versus hairy flagella, consider the following example: A hairy flagellum with l = 1.5 μm gives a time-averaged thrust of Fy,1.5 = 5.1 pN with a time-averaged power expenditure of P1.5 = 24 fW (Sec.…”

“…Predatory flagellates are important in aquatic food webs and the marine carbon cycle [3,[17][18][19], and their survival relies on the feeding flow generated by their hairy flagellum [20,21]. In hairy flagellates with two-dimensional flagellar wave motion, the tubular hairs are in the beat plane and perpendicular to the flagellum [22][23][24] [Fig.…”

Active sinking particles: sessile suspension feeders significantly alter the flow and transport to sinking aggregates

“…The density mismatch between aggregate and the surrounding fluid is calculated using scaling laws from Alldredge & Gotschalk [44] if not reported in the original reference. The point forces due to organisms used were approximately 2 pN for choanoflagellates [45], approximately 10 pN for nanoflagellates [46] and approximately 200 pN for V. convallaria [43] and Vorticella sp. [22].…”