The crown-filament pump of the suspension-feeding polychaete Sabella penicillus: filtration, effects of temperature, and energy cost

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The small-scale movements of cilia make the temperature-dependent viscosity of water a key physical/mechanical factor. In mussels and other suspension-feeding bivalves, bands of waterpumping lateral cilia produce the feeding current through the interfilamentary canals of the enlarged gill (which mainly serves as a water-pumping and food-particle collecting organ). Because the viscosity of seawater is inversely related to temperature, the linear increase of filtration rate with temperature in mussels cannot be explained solely by increased biological activity. To resolve the question of whether change in filtration rate with temperature in mussels Mytilus edulis is under mainly biological/physiological or physical/mechanical control, we conducted laboratory experiments on mussel-gill preparations stimulated with serotonin, and on intact mussels. In gill-preparations, the beat frequency of the water-pumping lateral cilia was measured both as a function of temperature and as a function of kinematic viscosity in dextran-and PVP-manipulated seawater at constant temperature. Data on kinematic viscosity of seawater and viscosity-manipulated seawater were converted to 'temperature equivalents' of seawater by measurement of the viscosities, and this showed that the effect of temperature on lateral cilia activity in gill-preparations is purely mechanical, controlled by the viscosity of the ambient seawater. Further, the ciliary beat frequency was found to depend on kinematic viscosity to the power -3/2 (f ≈ ν -3/2 ), a relation we used to develop a musselpump model for the filtration rate of intact mussels vs. viscosity. The model is in agreement with filtration rates measured in intact mussels, suggesting that viscosity of seawater is the controlling factor for the beat frequency of lateral pump-cilia and filtration rate in mussels. According to the model, the mussel pump yields a constant power within the temperature-tolerance interval.

Section: Discussionmentioning

confidence: 80%

Viscosity of seawater controls beat frequency of water-pumping cilia and filtration rate of mussels Mytilus edulis

Riisgård¹,

Larsen²

2007

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“…Downstream collecting has been studied in adult specimens of the polychaetes Sabella penicillus (Riisgård & Ivarsson 1990, Mayer 1994, Spirorbis tridentatus, the entoproct Loxosoma pectinaricola, and the cycliophore Symbion pandora . The ciliary bands show some general structural similarities in all groups, as appears from the descriptions that follow.…”

Section: Ciliary Downstream Collectingmentioning

confidence: 99%

Particle capture mechanisms in suspension-feeding invertebrates

Riisgård¹,

Larsen²

2010

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213

179

A large number of suspension-feeding aquatic animals (e.g. bivalves, polychaetes, ascidians, bryozoans, crustaceans, sponges, echinoderms, cnidarians) have specialized in grazing on not only the 2 to 200 µm phytoplankton but frequently also the 0.5 to 2 µm free-living bacteria, or they have specialized in capturing larger prey, e.g. zooplankton organisms. We review the different particle capture mechanisms in order to illustrate the many solutions to the common problem of obtaining nourishment from a dilute suspension of microscopic food particles. Despite the many differences in morphology and living conditions, particle capture mechanisms may be divided into 2 main types. (1) Filtering or sieving (e.g. through mucus nets, stiff cilia, filter setae), which is found in passive suspension feeders that rely on external currents to bring suspended particles to the filter, and in active suspension feeders that themselves produce a feeding flow by a variety of pump systems. Here the inventiveness of nature does not lie in the capture mechanism but in the type of pump system and filter pore-size. (2) A paddle-like flow manipulating system (e.g. cilia, cirri, tentacles, hair-bearing appendages) that acts to redirect an approaching suspended particle, often along with a surrounding 'fluid parcel', to a strategic location for arrest or further transport. Examples include (1) sieving (e.g. by microvilli in sponge choanocytes, mucus nets in polychaetes, acidians, and salps among others), filter setae in crustaceans, 'ciliary sieving' by stiff laterofrontal cilia in bryozoans and phoronids; and (2) 'cirri trapping' in mussels and other bivalves with eu-laterofrontal cirri, ciliary 'catch-up' in bivalve and gastropod veliger larvae, some polychaetes, entroprocts, and cycliophores. These capture mechanisms may involve contact with a particle, and possibly mechanoreception or chemoreception, or may include redirection of particles by the interaction of multiple currents (e.g. in scallops and other bivalves without eu-laterofrontal cirri). Based on the review, we discuss the current physical and biological understanding of the capture process and suggest a number of specific problems related to particle capture, which may be solved in the future using advanced theoretical, computational and experimental techniques.

“…Sabella penicillus. Upper: cross section of 2 pinnules with opposed compound lateral cilia in resting position at the end over recovery stroke, clc (1), and end of active stroke, clc (2); (fc, frontal cilia) (from Riisgård & Ivarsson 1990). Lower: retention spectrum expressed as relative clearance of particles of different sizes measured on the adult polychaete (from Jørgensen et al 1984) either not be caught-up or it is liable to roll off a single pushing cilium to subsequently be lost with the through flowing water.…”

Section: Structure Of Other Downstream Collecting Systemsmentioning

confidence: 99%

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

Riisgård¹,

Nielsen²,

Larsen³

2000

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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.