Filtration of submicrometer particles by pelagic tunicates

Abstract

Salps are common in oceanic waters and have higher per-individual filtration rates than any other zooplankton filter feeder. Although salps are centimeters in length, feeding via particle capture occurs on a fine, mucous mesh (fiber diameter d ∼0.1 μm) at low velocity (U = 1.6 ± 0.6 cm·s −1 , mean ± SD) and is thus a low Reynoldsnumber (Re ∼10 −3 ) process. In contrast to the current view that particle encounter is dictated by simple sieving of particles larger than the mesh spacing, a low-Re mathematical model of encounter rates by the salp feeding apparatus for realistic oceanic particle-size distributions shows that submicron particles, due to their higher abundances, are encountered at higher rates (particles per time) than larger particles. Data from feeding experiments with 0.5-, 1-, and 3-μm diameter polystyrene spheres corroborate these findings. Although particles larger than 1 μm (e.g., flagellates, small diatoms) represent a larger carbon pool, smaller particles in the 0.1-to 1-μm range (e.g., bacteria, Prochlorococcus) may be more quickly digestible because they present more surface area, and we find that particles smaller than the mesh size (1.4 μm) can fully satisfy salp energetic needs. Furthermore, by packaging submicrometer particles into rapidly sinking fecal pellets, pelagic tunicates can substantially change particle-size spectra and increase downward fluxes in the ocean.biofiltration | low Reynolds number | salps | colloids | carbon cycle F ilter feeding is a common strategy among marine plankton for collecting small food particles from a suspension. Pelagic tunicates in the class Thaliacea, order Salpida, have the highest perindividual filtration rates of all marine zooplankton filter feeders (1). Weight-specific clearance rates (70-4,153 mL·mg C −1 ·h −1 ) (2) are higher than most copepod and krill species. Salps filter feed by rhythmically pumping water into the oral siphon, through the pharyngeal chamber, and out the atrial siphon (Fig. 1A). This pumping action, generated by circular muscle bands, also creates a propulsive jet for locomotion. Food particles entering the pharyngeal chamber are strained through a mucous net that is continuously secreted and rolled into a food strand that moves posteriorly toward the esophagus. The bag-like net is secreted by the endostyle and fills much of the pharyngeal chamber (Fig. 1A). This feeding mechanism results in ingestion of any particles that enter the atrial siphon and adhere to the filtering mesh.After digestion, particles are packaged into dense fecal pellets, which often contain undigested or partially digested plankton (3, 4). These pellets remain intact for days (4) and have sinking speeds (200-3,646 m·d −1 ) (5, 6) that are higher than most copepod or krill pellets (3). Furthermore, diurnal vertical migration by some species may accelerate vertical export (7,8). The combination of high filtration rates, small mesh size, and rapid pellet sinking implies that salps have the potential to shift particle distributions toward larger sizes, con...

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