Downstream collecting in ciliary suspension feeders: the catch-up principle

Abstract

Based on observations of feeding structures and currents in the polychaete Spirorbis tridentatus, the entoproct Loxosoma pectinaricola and the cycliophore Symbion pandora, which all possess compound cilia, it is hypothesized that their capture mechanism is based on the catch-up principle. According to this principle, the compound cilia constitute the pump which generates a flow with suspended particles that enters the ciliary region. In this region the same cilia, during their power stroke, catch up with suspended particles and transfer the particles to a food groove, or a mouth cavity. In the particle-size retention spectrum, the lower limit depends on spacing between cilia in phase, while the upper end depends on cilia length which may or may not allow particles to enter the ciliary region. On the basis of fluid mechanical considerations and literature descriptions of structure and function of the ciliary bands of some rotifers and of the various types of trochophora larvae of annelids, molluscs and entoprocts, it is hypothesized that the feeding mechanisms of these organisms are based on the catch-up principle.

Trochophora larvae: Cell‐lineages, ciliary bands, and body regions. 1. Annelida and Mollusca

“…Planktotrophic larvae have a metatroch which is a postoral, peristomial band of compound cilia functioning in a downstream-collecting system together with the prototroch and the adoral ciliary zone (Nielsen, '87;Rouse, '99;Riisgård et al, 2000). A number of sabellid larvae have a metatroch and may capture particles, but mouth and gut are not fully developed and the particles are ''rejected'' at the mouth area and carried away along the gastrotroch (see above).…”

“…Many ''archaeogastropods'' have non-feeding planktonic larvae, but many ''mesogastropods'' have planktotrophic larvae with the characteristic downstream-collecting ciliary system of prototroch, adoral ciliary zone, and metatroch (Werner, '55;Riisgård et al, 2000). Several marine, most freshwater, and almost all terrestrial gastropods lay egg capsules in which the embryos go through a stage with a ciliated or unciliated velum before they emerge as small juveniles; this is ecologically described as direct development (Hickman,'99), but the presence of a seemingly non-functional larval velum strongly indicates that this is derived from the ancestral, indirect type of development with a planktotrophic larva (Hadfield and Iaea,'89).…”

Selective particle capture by asynchronously beating cilia

“…This is consistent with recent findings on a similar configuration which show that even for the particle sizes comparable to cilia movement, the difference between the motion of the fully resolved particles and that of passive tracers is small. 31 When the particles get in contact with cilia, based on recent observations that particles are captured by cilia moving in the flow direction, 10,32 we distinguish between two events: if a given particle is touched by the "front side" of the cilia, it gets captured. In biological systems, complex particle-organism interactions occur after downstream interception and the particle gets eventually removed from the capture region either directly or by other cilia and/or mouth-induced flows.…”

“…Particles need to be smaller than the space between cilia to pass through, and a cilium cannot encircle particles much larger than its length. 10 This thinking proved to be too simplistic. Our results show that the cilia beating coordination affects the particle-size spectrum in a nontrivial manner.…”

“…7 It is hypothesized that downstream particle collection is based on the "catch-up" principle. 10 According to this principle, cilia move the fluid with suspended particles into the ciliary region, where the same cilia, during their effective stroke, catch up with suspended particles and transfer them to a food groove or mouth cavity. A key point here is that capture takes place during the effective stroke when the "front side" of the cilium catches up with the particle.…”