Biol. Bull. 212: 93-103. (April 2007)
© 2007 Marine Biological Laboratory
Time and Extent of Ciliary Response to Particles in a Non-Filtering Feeding Mechanism
Richard R. Strathmann
Friday Harbor Laboratories and Department of Biology, University of Washington, 620 University Road, Friday Harbor, Washington 98250
E-mail: rrstrath{at}u.washington.edu
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Abstract
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Mechanisms of suspension feeding are usually described by the physics of inanimate filters. High-speed videorecordings in this study demonstrated that sea urchin larvae concentrate particles without filtration. They actively captured individual particles. At most times and places, the effective strokes of the swimming/feeding ciliary band were away from the circumoral field. Cilia of this band responded to particles by a reversal of beat that redirected the particle toward the circumoral field. A change of beat occurred along approximately 80 µm of ciliary band during particle capture. Cilia responded 0.02 to 0.06 s after the particle was within reach of effective strokes and reversed beat, usually for about 0.1 to 0.2 s. The whole event (disruption of forward beat) generally lasted between 0.13 and 0.5 s. These observations imply reversed movement of a parcel of water much larger than the included captured particle, but particles are nevertheless greatly concentrated because water is directed toward the circumoral field only when and where a particle is sensed. Thus most of the concentration of particles occurs by a temporarily and locally redirected current, without filtration, and size and quality of particles captured depends on sensory capabilities, not the mechanics of filtration.
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Introduction
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Suspension feeders cannot obtain their nutrition by merely drinking surrounding water because particulate food does not usually occur in dense suspension. Particles must be concentrated before they are ingested. Hypotheses for suspension-feeding mechanisms are commonly based on engineering models for filtration (Rubenstein and Koehl, 1977; LaBarbera, 1984; Shimeta and Jumars, 1991) or on encounters with single prey items (Gerritsen and Strickler, 1977; Rothschild and Osborn, 1988), but there are other possibilities. One is for an animal to sense a food item within its feeding current and briefly redirect part of the current so that a small parcel of water that includes the particle is redirected toward the mouth (Strathmann et al., 1972; Koehl and Strickler, 1981; Strathmann, 1982a; LaBarbera, 1984).
Sea urchin larvae capture particles with an induced local reversal of beat of a ciliary band that functions for both swimming and feeding. The ciliary reversals during captures were first described on the basis of high-speed cinefilms (Strathmann et al., 1972). The extent of the ciliary band that reversed beat was not observed, but other observations indicated that the reversal was local. The ciliary band is a continuous loop that extends up each arm and divides the body into a circumoral field (upstream from the band and including the mouth) and an aboral field (downstream from the band). Cilia beat away from the circumoral field during forward swimming. Freely swimming larvae, when feeding, retain particles at the upstream side of the ciliary band while continuing forward swimming. The captured particles are directed toward the circumoral field in the direction opposite to the prevailing current across the ciliary band. The continued forward swimming indicates that the reversed current is local, with beat elsewhere across the ciliary band unchanged during captures (Strathmann, 1971; Hart, 1991; Hart and Strathmann, 1994).
Supporting evidence for capture by ciliary reversals was provided by the observation that preventing ciliary reversal (by adding isosmotic magnesium chloride solution or by blocking calcium channels with cobalt ions) greatly reduced clearance rates (Strathmann, 1971; Hart, 1990). The nearly linear relation between maximum clearance rate (volume of water cleared of particles per unit time) and ciliary band length is consistent with retention of particles at the ciliary band (Hart, 1991, 1996a; Hart and Strathmann, 1994).
Physical mechanisms of suspension feeding must be inferred; they are not directly observed (Strathmann, 1982b; Hart, 1996b). Concentration of particles involves relative velocities of particles and water. Although dye or very small particles have been used to indicate the approximate location of concentration of particles (Strathmann, 1971; Strathmann et al., 1972), for practical reasons the flow of water at the spatial scale of particles and cilia is inferred from observations on cilia and particles. Inferences on suspension-feeding mechanisms are better if captures are directly observed and quantitatively analyzed; inferred mechanisms should be sufficient to explain observed clearance rates (Strathmann, 1982b; Hart 1990). High-speed video provides a quantitative record of rapid events. An advantage over previous observations with high-speed cine is that a larger number of captures can be targeted for quantitative analysis. The goals of this study were first to resolve times and spatial extent of ciliary responses to particles, then to draw inferences on the mechanism by which particles are concentrated.
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Materials and Methods
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Larval cultures were initiated from eggs and sperm of the sand dollar Dendraster excentricus (Eschscholtz, 1831). Larvae were reared on cultured algae, Rhodomonas sp., sometimes with the addition of Isochrysis galbana, in mechanically stirred cultures (Strathmann, 1987).
Particle capture was observed at room temperature (about 18 to 20 °C). The particles were cells of the alga Rhodomonas sp., which are about 10 µm long by 5 µm wide, exclusive of the flagella. Coverglasses were supported with plasticine (modeling clay) at the corners to form observation chambers just low enough to hold the plutei in place. Seawater and algae were introduced or removed at the edge of the coverglass. Observations of cilia were with a compound microscope with DIC optics and 20x and 40x objectives. Video recordings were with a Redlake Motionscope, at 250 frames s–1, so that the maximum resolution of timing of events was 4 ms. Recordings of about 2-s duration with a capture event included were transferred to a computer via an S-VHS-to-digital conversion. I recorded video clips from 11 larvae for views along an arm (with repeated observations for some larvae) and from 26 larvae for views through the band in optical section. I analyzed those clips in which particles were captured near the focal plane.
Use of 20x and 40x objectives reveals the activity of cilia during captures, but the field of view is small. Here captures were recorded in two views. For views with the beat of cilia in the plane of focus, captures were recorded at the loop of the ciliary band between postoral and posterodorsal arms (see short black bar in Fig. 1). For views with the ciliary band in the plane of focus and cilia moving through the plane of focus, captures were recorded along part of a postoral arm (see long black bar in Fig. 1).
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Figure 1. Capture of an algal cell by a pluteus. Time in milliseconds is at the lower left. The white arrow points to a cell of Rhodomonas sp. The algal cell was approaching the postoral arm at 0 ms, was at the ciliary band at 300 ms, had crossed to the other side of the arm at 400 ms, had recrossed the arm at 500 ms, and had entered the mouth at 750 ms. The cell was retained on the circumoral field at the upstream side of the ciliary band several times as it moved toward the mouth. The dark bars in the photo at time 0 indicate the portions of the ciliary band at which other captures were observed at higher magnification. The long dark bar indicates ciliary band along the arm and parallel to the optical plane. The short dark bar indicates the loop of the band between arms and perpendicular to the optical plane.
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With times resolved at 4-ms intervals and distances measured to about 0.75 µm, particle speeds were estimated to about ±0.1 mm s–1 for views with the ciliary beat in the plane of focus. Distances were measured to about 1.5 µm in views with the ciliary band in the plane of focus.
Particles are usually recaptured several times as they are transported toward the mouth. Because of the limited field of view at magnifications showing cilia, initial captures could rarely be distinguished from secondary captures during capture and transport of a particle. Cases in which a second capture of the algal cell occurred on a nearby portion of the ciliary band were not included in estimates of the extent of ciliary band response. Otherwise, no distinction was made between primary and secondary captures because observations had revealed no difference between them.
Tethering a swimming larva greatly enhances opportunities for observation, but the ensuing biases must be considered when interpreting data on times and velocities. Tethering can change the relative movement of cilia and particles (Emlet, 1990). This study's data for larvae held between slide and coverglass were therefore compared to Hart's (1996a) estimates of clearance rates measured for freely swimming larvae.
The described events are more easily seen in video records than in extracted frames. The video sequences are available at http://www.biolbull.org/supplemental/ but at reduced resolution because of compression.
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Results
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Captures at low magnification
Figure 1 illustrates capture of an algal cell with the whole larva in view, though the larva is confined by coverglass and slide. The cell is captured at the upstream side of the ciliary band. This cell was initially captured at the mid part of an arm (at 300 ms) and contacted the band at least four times as it was transported to the mouth. Transport often involves repeated captures at the ciliary band, and particles can be captured closer to an arm tip than in Figure 1 and transported greater distances to the mouth, with more of the repeated captures on the way.
Captures viewed with ciliary beat in the plane of focus
Captures of particles coincided with reversals of ciliary beat of short duration (Figs. 2, 3; Table 1). All particles captured were in the part of the current passing within the arc of the effective strokes of cilia of the band. Because the middle parts of effective strokes were not visible in recordings at this magnification and recording speed, the reach of cilia was estimated from the cilium length (about 25 µm). Distance of algal cells passing through the band was estimated from the bases of band cilia to the nearest part of the algal cell (Table 1). Most algal cells were stopped, with concomitant ciliary reversal, before they had moved more than halfway through the arc of effective strokes of the ciliary band. Some were stopped after passing more than halfway through the band, and a few were stopped after passing beyond reach of the cilia, with a belated ciliary reversal (Table 1). Times from an algal cell's coming within reach of the cilia to an observed change of beat varied. This variation included some error from estimating reach of cilia and a 4-ms resolution of event times, but there was clearly real variation in time to ciliary response (Table 1). An additional nine recorded captures with algal cells less in focus were similar except that in one case an algal cell that triggered a reversal was lost when the cilia resumed forward beat.
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Figure 2. Optical section through the ciliary band showing capture of an algal cell by a brief reversal of ciliary beat. Time in milliseconds is at the upper left. Horizontal arrows at 12 and 16 ms show direction of effective strokes of cilia, as inferred from direction of recovery strokes and confirmed by movement of the algal cell. Vertical arrowheads at 16 and 140 ms point to tips of extended cilia, visible presumably because their movement is slower during changes in direction of beat. At 0 ms, the algal cell, moving from the right of the figure, had been within reach of effective strokes of cilia for 16 to 20 ms; the curved recovery strokes indicate forward beat of cilia (effective beat toward the left of the figure). At 12 ms, ciliary beat was still forward; the algal cell was at the farthest left position recorded. At 16 ms, recovery strokes were reversed; the algal cell began to move to the right of the figure. At 104 ms, ciliary beat was still reversed and the algal cell had moved onto the circumoral field beyond reach of effective strokes of the ciliary band. At 140 ms, cilia were in transition to forward beat. The reversal had lasted 124 ms. By 200 ms, forward beat was re-established, as indicated by direction of recovery strokes, and the algal cell was out of the frame. The diagram shows single cilia in their recovery strokes (or momentarily arrested at 140 ms) and direction of movement of the algal cell during the videorecording described above.
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Figure 3. Optical section through the ciliary band showing capture of an algal cell passing just within reach of the cilia. Time in milliseconds is at the lower right. At 0 ms, the algal cell had moved into view in the forward current and was just within the length of cilia of the band (about 25 µm). At 20 ms, the cilia were still in forward beat (effective strokes down in the figure), as indicated by curvature of recovery strokes. At 24 ms, the cilia were beginning to change form of beat. At 28 ms, beat had reversed, as indicated by the curvature of recovery strokes. The algal cell moved little during the change from forward to reversed beat (20 to 28 ms). The algal cell moved toward the circumoral field in the reversed current more slowly during the 36 ms between 28 and 64 ms than in the next 36 ms from 64 to 100 ms, indicating an increasing velocity of the reversed current. The diagram shows single cilia in their recovery strokes and direction of movement of the algal cell during the videorecording described above.
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The maximum speeds of algal cells in the forward ciliary current before capture were similar to their maximum speeds in the reversed ciliary current during capture, about 1 mm s–1 (Table 1). The single observation of capture of an algal cell after it had passed through the band was also the observation with the fastest current speed (Table 1). An even faster speed (e.g., 2.6 mm s–1) was recorded when a pluteus did not respond to an algal cell with a ciliary reversal (Fig. 4).
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Figure 4. Algal cell passing the ciliary band without capture and without reversal of ciliary beat. The cell was within 21 µm from the bases of cilia and therefore within reach of cilia in their effective strokes. Time in milliseconds is at the upper right.
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The transition from forward to reversed beat was rapid. The motion of the algal cell and the curvature of recovery strokes indicated the beginning of reversed beat. The increase in speed of the algal cell during the first part of its reversed trajectory indicated the time from stopped forward motion to a fully organized reversed beat of cilia (Fig. 3).
The duration of clearly reversed ciliary beat was on the order of 0.1 s in half the captures and longer in the others (Table 1). The duration of change of beat during the whole capture (including transitions) was less than 0.3 s in more than half the captures and rarely exceeded 0.4 s.
The transition from reversed beat to regular forward beat was longer than that for forward to reverse and varied greatly in duration, which accounts for the large and varying difference between duration of steady reversed beat and the entire period of disrupted forward beat in Table 1. Duration of the transition from reversed to forward beat was estimated from frames with cilia extended but not in rapid effective strokes (Fig. 2 at 140 ms) and by curvature of cilia in the direction of forward or reversed recovery strokes. Some of the variation in the transition from reverse to forward is error from difficulty in judging when beat has become regularly forward. When the particle has been transported off-frame, there is no current marker. But real variation in timing of restoration of forward beat was apparent.
Captures viewed with ciliary band in the plane of focus
During captures, ciliary beat changed along an extent of the ciliary band much larger than the diameter of the captured algal cell. In some cases the cilia disappeared from focus during disruption of beat (Fig. 5), and in others the pattern of extensions of the beating cilia changed (Fig. 6). The mean length of band affected at maximal disruption of beat was 76 ± 24 µm (mean ± SD, n = 8), estimated from captures in which the entire length of band with changed ciliary beat was in focus and within the field of view. Distances of changed beat along the band were similar on both sides of the captured cell. For a larger sample, in which distance was measured to just one side of the algal cell (either proximally or distally), the estimate was 40 ± 10 µm (n = 24), about half the estimate for total length of band affected. The extent of band affected had an estimated range of 45 to 112 µm (n = 8). Difficulties in distinguishing an exact boundary to the length of band with changed beat may have contributed somewhat to this variation. Figure 5 shows the spatial spread of disrupted forward beat along the ciliary band and then the subsequent reduction of the extent of ciliary band affected. In two successive captures of this algal cell by this pluteus, the duration of disrupted beat was 0.21 and 0.25 s. This estimate is consistent with observations with ciliary beat in the plane of focus (Table 1). The capture in Figure 6 illustrates the timing, relative to position of the algal cell, from disruption of beat to the transition toward resumption of usual beat at the end of the recorded interval.
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Figure 5. Extent of change in ciliary beat during capture of an algal cell. Time in milliseconds is at the upper left. The white bar indicates the approximate extent of changed beat along the band. The algal cell approached the ciliary band at 0 ms, reached the part of the arc through the ciliary band that is farthest from the arm at 16 ms, and still had not triggered a change in ciliary beat at 32 ms. At 36 ms, the disappearance of visible cilia near the algal cell indicated the beginning of change in ciliary beat. At 48 ms, cilia had changed beat over a greater length of the band, and the algal cell was at the part of the arc farthest from the arm in its return toward the frontal side of the arm. At 80 ms, the algal cell passed onto the frontal surface of the arm; the extent of changed beat along the band was about 50 µm. At 252 ms, the algal cell was at its greatest distance from the other side of the arm (where it was captured again). At 308 ms, the extent of the ciliary band that had not returned to forward beat had diminished. At 344 ms, the cilia at the point of capture had returned to their usual beat.
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Figure 6. Timing of change in ciliary beat during capture of an algal cell. Time in milliseconds is at the upper left. The algal cell was at the ciliary band at 0 ms and moved away from the arm in the forward ciliary current at 32 and 44 ms, while the beat of cilia remained unchanged. At 48 ms, a change in the beat of cilia was just beginning and became more clearly visible at 52 ms. (The change in ciliary beat was manifested as less visible cilia in the vicinity of the algal cell in the photos at 52 to 100 ms.) At 64 and 68 ms, the algal cell moved back toward the arm in the reversed ciliary current. At 100 ms, the algal cell had been moved to the frontal surface of the arm. At 156 ms, the algal cell had been moved to the other side of the arm and the cilia at the site of capture were returning to their usual beat.
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Discussion
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These observations document the timing and spatial extent of the induced reversals of ciliary beat associated with particle capture. A stimulus from a particle is the only hypothesis that accounts for a reversal of beat so localized in time and place.
The extent of the ciliary band that responds to the particle (observations with the band in the focal plane) and the duration of reversed beat of cilia (observations with ciliary beat in the focal plane) imply that a volume of water much larger than the particle is redirected toward the circumoral field. A minority of the responding cilia may or may not contact a captured particle, but what moves captured particles and concentrates them is a brief locally reversed current. Particles are greatly concentrated because the volume of water so redirected is small compared to the flow elsewhere across the band, and the reversed flow is brief (Hart and Strathmann, 1995). Hence forward swimming is not interrupted during captures.
Capture of a particle depends on a stimulus and a response. The relative rates of capture of particles differing in size or other qualities cannot be predicted from filtration theory (Rubenstein and Koehl, 1977; LaBarbera, 1984; Shimeta and Jumars, 1991). The effect of particle size, shape, and possibly other qualities on the ciliary response has no necessary and fixed relationship to predictions based on filtration processes such as sieving, direct interception, and adhesion. The initial and largest concentration of suspended particles is achieved without this kind of filter. What determines capture is the stimulus that prompts reversal of cilia.
One hypothesis for the stimulus is that a particle increases drag on cilia whose effective strokes are close to the particle. The angular velocities of effective strokes have not been observed for plutei, but velocities of compound cilia in their effective strokes exceed the mean velocity of particles passing through a ciliary band (Strathmann and Leise, 1979; Emlet, 1990; Riisgård et al., 2000). Thus the cilia may encounter increased resistance as effective strokes overtake particles. There is as yet no evidence for a chemical stimulus for local reversals at the ciliary band. Comparisons of rates of capture of algal-flavored and unflavored plastic spheres indicated that captures at the ciliary band did not depend on chemical stimuli although acceptance or rejection nearer to the mouth did, thus supporting the hypothesis of a mechanical stimulus for the local reversals that retain particles at the ciliary band (Appelmans, 1994).
Substitution of magnesium ions, reduced concentration of calcium ions, and blockage of ion channels with cobalt ions block ciliary reversals in general and also capture of particles at the ciliary band (Strathmann, 1971; Hart, 1990; Wada et al., 1997). An influx of calcium ions appears to be involved in ciliary reversal (Degawa et al., 1986; Hart, 1990). A plausible hypothesis is that the particle stimulates an influx of calcium ions, producing a reversal in the immediately affected cells. Because there is only one cilium per cell (Strathmann, 1971), the stimulus must also be transmitted to neighboring cells. Propagation of an action potential to neighboring cells is a possibility (Mackie, 1970; Spencer, 1974; Murakami, 1989). Interaction between cilia is another possibility, but something else must then be proposed as a limit on the extent of propagation along the ciliary band.
The frequency with which particles of a given kind induce a reversal and capture varies with degree of satiation, temperature, and other factors (Strathmann, 1971; Hart, 1990, 1991, 1996b; Hart and Strathmann, 1994). Individual echinoderm larvae clearly vary clearance rate at the initial capture at the ciliary band as well as later, by rejection (Strathmann, 1971). Neurotransmitters modify ciliary beating of plutei (Lacalli and Gilmour, 1990; Wada et al., 1997), and axons are associated with the ciliary band of plutei, other echinoderm larvae, and hemichordate larvae (Burke, 1983; Dautov and Nezlin, 1992; Chee and Byrne, 1999; Beer et al., 2001; Lacalli and Gilmour, 2001; Lacalli and Kelly, 2002; Nakajima et al., 2004a, b). A plausible hypothesis is that the responsiveness of the cilia is under neural control. I know of no studies of how transmitters or other processes modulate the local responses of cilia of the ciliary band to stimuli from particles.
None of the processes hypothesized here for an induced local reversal of beat are novel. Response of cilia to mechanical stimuli, neural modulation of ciliary beat, and intercellular propagation of a calcium wave together with change of ciliary beat are features of ciliary responses to stimuli that are known from other animal systems (Lowe, 1997; Lansley and Sanderson, 1999).
The limits on sensing particles appear to differ among species. Echinoderm larvae from temperate and warm waters capture small (<2 µm) particles at a lower rate than large (>10 µm) particles, which is consistent with a limit on response that is associated with the magnitude of the stimulus (Ayukai, 1994; Hart and Strathmann, 1995; Okaji et al., 1997), but echinoderm larvae in Antarctic waters capture bacteria-size particles at not such a reduced rate relative to captures of larger particles (Bosch et al., 1990; Pearse et al., 1991). The hypothesis that the mechanical stimulus is greater at the higher viscosities in colder waters is not supported by experimental manipulation of viscosity; capture of 2-µm particles was reduced relative to 10-µm particles at greater viscosities (Podolsky, 1994). Moreover, the increased drag for cilia encountering a particle depends on both viscosity and velocity of the cilia. Temperature has opposite effects on viscosity and ciliary current velocities (Podolsky and Emlet, 1993). Also, the difference in velocities of cilia and particles, and hence the stimulus, may decrease with slower current and greater viscosity. Another possibility is that an adaptation to scarce particulate food is a response to a smaller change in drag, but this adaptation is not apparent in studies of larvae of an echinoderm from warm waters with low particle concentrations (Ayukai, 1994; Okaji et al., 1997).
Induced local reversals of beat at the ciliary band are not the only mechanism by which sea urchin larvae concentrate particles before ingesting them. When reversals are blocked, some particles enter the oral cavity directly, and these paths account for about 5% of the maximum clearance rate (Hart, 1990). Also, most of the water diverted toward the mouth by local ciliary reversals is not swallowed. The packing of particles in the esophagus indicates particles are further concentrated in the oral cavity before they are passed to the stomach. Mucus may play a role in this further concentration of particles. Particles ejected from the esophagus are bound in mucus, in contrast to particles that are rejected or lost before they enter the mouth (Strathmann, 1971). Nevertheless, when food is scarce, captures at the ciliary band account for most of the concentration of suspended particles before ingestion.
The current speeds estimated for the nine captures in which the algal cell was near the focal plane (Table 1) were close to Hart's (1996a) estimate of 1.16 ± 0.14 SD mm s–1 for particles passing near the tips of cilia of these larvae. Estimates by Emlet and Strathmann (1994) were somewhat greater. Differences in temperature and responses of larvae to conditions on a microscope slide could explain the differences.
Particle speeds did not increase toward the cilium tip. This observation contrasts with maximum particle speeds near or just short of tips of the large compound cilia in preoral ciliary bands of feeding mollusc larvae (Strathmann and Leise, 1979; Gallager, 1988; Emlet, 1990). However, for bands of simple cilia of mitraria larvae of an owenid polychaete and of plutei of Dendraster excentricus, the scatter in plots of particle speeds versus distance along cilia obscured any gradient in velocities from outer edge of recovery strokes to cilium tips (Emlet and Strathmann, 1994).
Holding the pluteus between slide and coverglass could affect current speeds even within the sweep of cilia, but the observed velocities are more than sufficient to account for the maximum clearance rates estimated for plutei swimming freely in much larger chambers (Hart, 1996a). There is a zone of about 20 µm where the effective strokes extend beyond the recovery strokes. An average current of 0.42 mm s–1 passing through this zone would account for Hart's estimated clearance rate of about 1 µl min–1 per 2 mm of ciliary band. This factor of 2 difference is similar to previous comparisons of direct observation of ciliary currents and captures by freely swimming plutei (Hart, 1996b). Any of several causes could account for the higher observed current speeds, despite tethering and drag from coverslip and slide. Temperature differences could account for much of the difference in observed current speeds (Podolsky and Emlet, 1993), because Hart's (1996a) estimates of maximum clearance rates were in a cooled chamber several degrees Celsius below the temperatures at which I measured current speeds. Other factors might contribute to this difference in estimates: currents past the loop of the band between arms might be faster than elsewhere along the band; estimates of maximum clearance rates, even when based on direct observations, might be low; plutei might not respond to algal cells as often as in the videorecorded sample of events, which selected captures in preference to no capture.
Baba and Mogami (1987) estimated the period from stimulus to earliest response in ciliary reversal to be 9.5 ms for the earliest response and 16 ms for tip angle. (Their estimates were for cilia on a different species of pluteus, presumably on a different location on the larva, and at 19 to 21°C.) This response time is much less than their estimated duration of > 100 ms for a single beat cycle of effective and recovery stroke in forward beat. It is also less than my estimate of 16 to 60 ms for the period between a particle's first coming within reach of the cilia and its stopping forward motion, with concomitant ciliary reversal (Table 1). Thus reported times from stimulus to reversal can account for speed of response in particle capture. The reversed beat during captures differed in form from the forward beat of the cilia, as indicated by the recovery strokes, with a broader curve during reversals (Fig. 3). Mogami et al. (1993) described a similar difference between forward and reversed strokes of cilia on isolated cells from echinoplutei. My estimate for transition between reversed and forward strokes (Fig. 2, 140 ms) was similar to that described for epaulette cilia of plutei (Mogami et al., 1991).
Although high-speed recordings are lacking for ciliary feeding by larvae of other echinoderm classes and of hemichordates, the morphology of ciliary bands and the particle paths near feeding and non-feeding larvae suggest that these larvae also capture particles by an induced local reversal of beat (Strathmann, 1971; Strathmann and Bonar, 1976; Hart, 1991, 1996b; Hart et al., 1994). These are the only larvae known to feed with this simple an arrangement of ciliary bands. The inference from genetic sequence data is that the echinoderms and hemichordates are a monophyletic group (Peterson, 2004; Smith et al., 2004; Zeng and Swalla, 2005). Upstream capture by induced local reversals of a single band of cilia could be a derived ancestral character for this clade.
There is, however, a similar ciliary mechanism in another group of animals. Local induced changes of beat also contribute to capture of particles by brachiopods and bryozoans, and particle paths suggest that the changes of beat are reversals (Strathmann, 1982a, 2005, 2006). Here also a brief local reversal of current is a mechanism of concentration, although the stimulus may be interception by upstream laterofrontal cilia. Inferences from DNA sequence data place these lophophorate phyla in a different clade of bilaterians, the lophotrochozoa (Halanych, 2004). These animals also employ sieving by a laterofrontal band of cilia (Strathmann and McEdward, 1986; Nielsen and Riisgård, 1998; Larsen and Riisgård, 2002; Strathmann, 2005, 2006) as well as local changes of beat of their lateral cilia (Strathmann, 1982a, 2005, 2006). Either the mechanism of particle capture by induced changes in beat is very ancient or it evolved at least twice: once as a mechanism of capture by a single ciliary band and once as one of the mechanisms of capture by parallel lateral and laterofrontal ciliary bands.
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Acknowledgments
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NSF grant OCE 0217304 and the Friday Harbor Laboratories of the University of Washington supported this research. I am grateful to D. Schiopu for her observations of particle capture by plutei that stimulated this study and to M. F. Strathmann and M. LaBarbera for advice.
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Footnotes
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Received 18 April 2006; accepted 4 December 2006.
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Literature Cited
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Appelmans, N. 1994. Sites of particle selection determined from observations of individual feeding larvae of the sand dollar Dendraster excentricus. Limnol. Oceanogr. 39: 404–411.
Ayukai, T. 1994. Ingestion of ultraplankton by the planktonic larvae of the crown-of-thorns starfish, Acanthaster planci. Biol. Bull. 186: 90–100.[Abstract]
Baba, S. A., and Y. Mogami. 1987. High time-resolution analysis of transient bending patterns during ciliary responses following electric stimulation in sea urchin embryos. Cell Motil. Cytoskel. 7: 198–208.[ISI]
Beer, A.-J., C. Moss, and M. Thorndyke. 2001. Development of serotonin-like and SALMFamide-like immunoreactivity in the nervous system of the sea urchin Psammechinus miliaris. Biol. Bull. 200: 268–280.[Abstract/Free Full Text]
Bosch, I., J. S. Pearse, and L. V. Basch. 1990. Particulate food and growth of planktotrophic sea star larvae in McMurdo Sound, Antarctica. Antarct. J. US 25: 210–211.
Burke, R. D. 1983. Development of the larval nervous system of the sand dollar, Dendraster excentricus. Cell Tissue Res. 229: 145–154.[ISI][Medline]
Chee, F., and M. Byrne. 1999. Development of the larval serotonergic nervous system in the sea star Patiriella regularis as revealed by confocal imaging. Biol. Bull. 197: 123–131.[Abstract]
Dautov, S. Sh., and L. P. Nezlin. 1992. Nervous system of the tornaria larva (Hemichordata, Enteropneusta). A histochemical and ultrastructural study. Biol. Bull. 183: 463–475.[Abstract]
Degawa, M., Y. Mogami, and S. A. Baba. 1986. Developmental changes in Ca2+ sensitivity of sea urchin embryo cilia. Comp. Biochem. Physiol. 85A: 83–90.
Emlet, R. B. 1990. Flow fields around ciliated larvae: effects of natural and artificial tethers. Mar. Ecol. Prog. Ser. 63: 211–225.
Emlet, R. B., and R. R. Strathmann 1994. Functional consequences of simple cilia in the mitraria of oweniids (an anomalous larva of an anomalous polychaete) and comparisons with other larvae. Pp. 143–157 in Reproduction and Development of Marine Invertebrates, W. H. Wilson, S. A. Stricker, and G. L. Shinn, eds. Johns Hopkins University Press, Baltimore.
Gallager, S. M. 1988. Visual observations of particle manipulation during feeding in larvae of a bivalve mollusk. Bull. Mar. Sci. 43: 344–365.
Gerritsen, J., and J. R. Strickler. 1977. Encounter probabilities and community structure in zooplankton: a mathematical model. J. Fish. Res. Board Can. 34: 73–82.
Halanych, K. M. 2004. The new view of animal phylogeny. Annu. Rev. Ecol. Evol. Syst. 35: 229–256.
Hart, M. W. 1990. Manipulating external Ca2+ inhibits particle capture by planktotrophic echinoderm larvae. Can. J. Zool. 68: 2610–2615.
Hart, M. W. 1991. Particle captures and the method of suspension feeding by echinoderm larvae. Biol. Bull. 180: 12–27.[Abstract]
Hart, M. W. 1996a. Variation in suspension feeding rates among larvae of some temperate, eastern Pacific echinoderms. Invertebr. Biol. 115: 30–45.
Hart, M. W. 1996b. Deconstructing suspension feeders by analysis of film and video. Invertebr. Biol. 115: 185–190.
Hart, M. W., and R. R. Strathmann. 1994. Functional consequences of phenotypic plasticity in echinoid larvae. Biol. Bull. 186: 291–299.[Abstract]
Hart, M. W., and R. R. Strathmann. 1995. Mechanisms and rates of suspension feeding. Pp. 193–221 in Ecology of Marine Invertebrate Larvae, L. McEdward, ed. CRC Press, Boca Raton, FL.
Hart, M. W., R. L. Miller, and L. P. Madin. 1994. Form and feeding mechanism of a living Planctosphaera pelagica (phylum Hemichordata). Mar. Biol. 120: 521–533.
Koehl, M. A. R., and J. R. Strickler. 1981. Copepod feeding currents: food capture at low Reynolds number. Limnol. Oceanogr. 26: 1062–1093.
LaBarbera, M. L. 1984. Feeding currents and particle capture mechanisms in suspension feeding animals. Am. Zool. 24: 71–84.[ISI]
Lacalli, T. C., and T. H. J. Gilmour. 1990. Ciliary reversal and locomotory control in the pluteus larva of Lytechinus pictus. Phil. Trans. R. Soc. Lond. B 330: 391–396.[ISI]
Lacalli, T. C., and T. H. Gilmour. 2001. Locomotory and feeding effectors of the tornaria larva of Balanoglossus biminiensis. Acta Zool. 82: 117–126.
Lacalli, T. C., and S. J. Kelly. 2002. Anterior neural centres in echinoderm bipinnaria and auricularia larvae: cell types and organization. Acta Zool. 83: 99–110.
Lansley, A. B., and M. J. Sanderson. 1999. Regulation of airway ciliary activity by Ca2+: simultaneous measurement of beat frequency and intracellular Ca2+. Biophys. J. 77: 629–638.[ISI][Medline]
Larsen, P. S., and H. U. Riisgård. 2002. On ciliary sieving and pumping in bryozoans. J. Sea Res. 48: 181–195.
Lowe, B. 1997. The role of Ca2+ in deflection-induced excitation of motile, mechanoresponsive balancer cilia in the ctenophore statocyst. J. Exp. Biol. 200: 1593–1606.[Abstract]
Mackie, G. O. 1970. Neuroid conduction and the evolution of conducting tissues. Q. Rev. Biol. 45: 319–332.[Medline]
Mogami, Y., K. Fujima, and S. A. Baba. 1991. Five different states of ciliary activity in the epaulette of echinoplutei. J. Exp. Biol. 155: 65–75.[ISI]
Mogami, Y., S. Sekiguchi, and S. A. Baba. 1993. Beating of cilia of sea urchin embryos: a critical comparison of the normal and reversed beating of cilia of isolated cells. J. Exp. Biol. 175: 251–266.[Abstract]
Murakami, A. 1989. The control of cilia in metazoa: ciliary functions and Ca-dependent responses. Comp. Biochem. Physiol. 94A: 375–382.[Medline]
Nakajima, Y., T. Humphreys, H. Kaneko, and K. Tagawa. 2004a. Development and neural organization of the tornaria larva of the Hawaiian hemichordate, Ptychodera flava. Zool. Sci. 21: 69–78.[ISI][Medline]
Nakajima, Y., H. Kaneko, G. Murray, and R. D. Burke. 2004b. Divergent patterns of neural development in larval echinoids and asteroids. Evol. Dev. 6: 95–104.[ISI][Medline]
Nielsen, C., and H. U. Riisgård. 1998. Tentacle structure and filter-feeding in Crisia eburnea and other cyclostomatous bryozoans, with a review of upstream-collecting mechanisms. Mar. Ecol. Prog. Ser. 168: 163–186.
Okaji, K., T. Ayukai, and J. S. Lucas. 1997. Selective feeding by larvae of the crown-of-thorns starfish, Acanthaster planci (L.). Coral Reefs 16: 47–50.[Medline]
Pearse, J. S., I. Bosch, V. B. Pearse, and L. V. Basch. 1991. Differences in feeding on algae and bacteria by temperate and Antarctic seastar larvae. Antarct. J. US 26: 170–172.
Peterson, K. J. 2004. Isolation of Hox and Parahox genes in the hemichordate Ptychodera flava and the evolution of deuterostome Hox genes. Mol. Phylogenet. Evol. 31: 1208–1215.[ISI][Medline]
Podolsky, R. D. 1994. Temperature and water viscosity: physiological versus mechanical effects on suspension feeding. Science 265: 100–103.[Abstract/Free Full Text]
Podolsky, R. D., and R. B. Emlet. 1993. Separating the effects of temperature and viscosity on swimming and water movement by sand dollar larvae (Dendraster excentricus). J. Exp. Biol. 176: 207–221.[Abstract]
Riisgård, H. U., C. Nielsen, and P. S. Larsen. 2000. Downstream collecting in ciliary suspension feeders: the catch-up principle. Mar. Ecol. Prog. Ser. 207: 33–51.
Rothschild, B. J., and T. R. Osborn. 1988. Small-scale turbulence and plankton contact rates. J. Plankton Res. 10: 465–474.[Abstract/Free Full Text]
Rubenstein, D. I., and M. A. R. Koehl. 1977. The mechanisms of filter feeding: some theoretical considerations. Am. Nat. 111: 981–994.[ISI]
Shimeta, J., and P. A. Jumars. 1991. Physical mechanisms and rates of particle capture by suspension-feeders. Oceanogr. Mar. Biol. Annu. Rev. 29: 191–257.
Smith, A. B., K. J. Peterson, G. Wray, and D. T. Littlewood. 2004. From bilateral symmetry to pentaradiality: the phylogeny of hemichordates and echinoderms. Pp. 365–383 in Assembling the Tree of Life, J. Cracraft and M. J. Donoghue, eds. Oxford University Press, Oxford.
Spencer, A. N. 1974. Non-nervous conduction in invertebrates and embryos. Am. Zool. 14: 917–929.[ISI]
Strathmann, M. F. 1987. Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast. University of Washington Press, Seattle. 670 pp.
Strathmann, R. R. 1971. The feeding behavior of planktotrophic echinoderm larvae: mechanisms, regulation, and rates of suspension feeding. J. Exp. Mar. Biol. Ecol. 6: 109–160.
Strathmann, R. R. 1982a. Cinefilms of particle capture by an induced local change of beat of lateral cilia of a bryozoan. J. Exp. Mar. Biol. Ecol. 62: 225–236.[ISI]
Strathmann, R. R. 1982b. Comment on Dr. Gilmour's views on feeding by hemichordates and lophophorates. Can. J. Zool. 60: 3466–3468.
Strathmann, R. R. 2005. Ciliary sieving and active ciliary response in capture of particles by suspension-feeding brachiopod larvae. Acta Zool. 86: 41–54.
Strathmann, R. R. 2006. Versatile ciliary behaviour in capture of particles by the bryozoan cyphonautes larva. Acta Zool. 87: 83–89.
Strathmann, R. R., and D. Bonar. 1976. Ciliary feeding of tornaria larvae of Ptychodera flava (Hemichordata: Enteropneusta). Mar. Biol. 34: 317–324.
Strathmann, R. R., and E. Leise. 1979. On feeding mechanisms and clearance rates of molluscan veligers. Biol. Bull. 157: 524–535.[Abstract/Free Full Text]
Strathmann, R. R., and L. R. McEdward. 1986. Cyphonautes ciliary sieve breaks a biological rule of inference. Biol. Bull. 171: 694–700.[Abstract/Free Full Text]
Strathmann, R. R., T. L. Jahn, and J. R. C. Fonseca. 1972. Suspension feeding by marine invertebrate larvae: clearance of particles by ciliated bands of a rotifer, pluteus, and trochophore. Biol. Bull. 142: 505–519.[Abstract/Free Full Text]
Wada, Y., Y. Mogami, and S. A. Baba. 1997. Modification of ciliary beating in sea urchin larvae induced by neurotransmitters: beat-lane rotation and control of frequency fluctuation. J. Exp. Biol. 200: 9–18.[Abstract]
Zeng, L., and B. L. Swalla. 2005. Molecular phylogeny of the protochordates: chordate evolution. Can. J. Zool. 83: 24–33.
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Abstract
Introduction
