Dynamic sinking behaviour in marine phytoplankton: rapid changes in buoyancy may aid in nutrient uptake

Abstract

Phytoplankton sinking is an important property that can determine community composition in the photic zone and material loss to the deep ocean. To date, studies of diatom suspension have relied on bulk measurements with assumptions that bulk rates adequately capture the essential characteristics of diatom sinking. However, recent work has illustrated that individual diatom sinking rates vary considerably from the mean bulk rate. In this study, we apply high-resolution optical techniques, individual-based observations of diatom sinking and a recently developed method of flow visualization around freely sinking cells. The results show that in both field samples and laboratory cultures, some large species of centric diatoms are capable of a novel behaviour, whereby cells undergo bursts of rapid sinking that alternate with near-zero sinking rates on the timescales of seconds. We also demonstrate that this behaviour is under direct metabolic control of the cell. We discuss these results in the context of implications for nutrient flux to the cell surface. While nutrient flux in large diatoms increases during fast sinking, current mass transport models cannot incorporate the unsteady sinking behaviour observed in this study. However, large diatoms appear capable of benefiting from the enhanced nutrient flux to their surface during rapid sinking even during brief intervening periods of near-zero sinking rates.

Keywords: diatom; nutrient flux; phytoplankton; sinking.

Figure 1.

Instantaneous sinking speeds of representative individual cells from a wild-collected sample shows three species of centric diatoms exhibiting the start–stop sinking behaviour. (a) Coscinodiscus radiatus. (b) Coscinodiscus wailesii. (c) Palmerina hardmaniana.

Figure 2.

Sinking behaviour of individual cultured C. wailesii cells that are representative of the population means for each experimental condition. (a) Instantaneous sinking speed. (b) Cumulative sinking distance over a 30 s period (25 mm field of view).

Figure 3.

Histograms show the frequency of instantaneous sinking rates measured from populations of C. wailesii under various levels of nutrient stress over a 1 min period. (a) Nutrient replete (n = 69), (b) 2 days in FSW (n = 70), (c) 6 days in FSW (n = 72).

Figure 4.

Instantaneous sinking speeds of representative Coscinodiscus wailesii cells during and after inhibitor treatments using manually computed µPIV corrections. Dotted lines show cells that have been exposed to the inhibitor and solid lines shows the start–stop sinking behaviour is regained after cells have been rinsed with filtered seawater. (a) Myosin ATPase inhibitor, 2,3 butanedione monoxime (BDM). (b) Actin inhibitor (latrunculin A).

Figure 5.

Flow fields measured around a freely sinking C. wailesii. The colour-coded arrows represent water velocity corrected for local turbulent flow. Zero flow is relative to a fixed point in the x,y,z space away from the cell in the experimental chamber. The two-dimensional vectors also include values from movement in the third dimension. (a) Slow sinking phase (0.04 mm s⁻¹). (b) Fast sinking phase (0.21 mm s⁻¹) of the same cell 0.3 s later. Note the displacement of fluid as the cell sinks, the replacement of fluid behind the cell and velocity gradient of the water laterally adjacent to the cell. This creates the streamline effect presented in the typical presentation of a fixed particle with water flowing past it.

Figure 6.

Cell motion and mass transport. (a) Relationship between the Péclet number (Pe), which is a function of cell sinking speed, and the Sherwood number (Sh) redrawn from Karp-Boss et al. (dotted line). Overlaid are the population means for nutrient replete cells (n = 69) and for cells kept in FSW for 2 (n = 70) or 6 days (n = 72). Triangles represent the mean minimum sinking speed (slow sinking state or ‘stop’ phase) for each condition, circles represent the population average of both slow and fast sinking states, and squares represent the mean maximum sinking speed (fast sinking state or ‘start’ phase). Note: these values only represent the Pe and Sh of a cell sinking at a steady speed for each condition listed. (b) Conceptual relationship between the average sinking speed of a large centric diatom and the potential increase in mass transport owing to sinking rates. Dotted line represents a constantly sinking cell and the solid line represents a cell exhibiting the start–stop sinking behaviour.