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Functional and Evolutionary Implications of Opposed Bands, Big Mouths, and Extensive Oral Ciliation in Larval Opheliids and Echiurids (Annelida).

BENJAMIN G. MINER [1]

ERIC SANFORD [2]

RICHARD R. STRATHMANN [3]

BRUNO PERNET [3]

RICHARD B. EMLET [4]

Abstract. Larvae of two annelids, the opheliid Armandia brevis and the echiurid Urechis caupo, captured small particles between opposed prototrochal and metatrochal ciliary bands and also captured large particles with wide ciliated mouths. The body volume of larval A. brevis increased more rapidly than the estimated maximum clearance rate as segments were added. Capture of larger particles by late-stage larvae may compensate for this potentially unfavorable allometry. The existence of larvae that use two feeding mechanisms at once, not previously known in annelids, suggests possible evolutionary routes between larval forms that feed only with opposed bands (e.g., serpulids and oweniids) and those that use complex oral ciliature to feed primarily on large particles (e.g., polynoids and nephtyids). In particular, the metatroch and food groove of opposed-band feeders may have arisen as expansions of oral ciliation in ancestral large-particle feeders; alternatively, extensive oral ciliation in large-particle feed ers may have originated as a modification of metatroch and food-groove cilia in ancestral opposed-band feeders.

Introduction

The trochophore is a larval form of several phyla: Annelida, Sipuncula, Mollusca, and Entoprocta (Nielsen, 1995). It is largely defined by the presence of the prototroch, a preoral ciliary band with a well-defined cell lineage. Despite this and other embryological similarities, trochophores are structurally and functionally diverse. Much of this diversity is found among the approximately 70 families of annelids in which larvae occur. Annelid larvae vary in the number and position of ciliary bands (though almost all possess a prototroch), and in whether or not they feed. Among annelid larvae that feed, mechanisms of capturing suspended particles have been described in only a few species (Strathmann, 1987).

One of these feeding mechanisms involves capturing and transporting particles with the prototroch and several postoral ciliary bands. The prototroch beats with an anterior-to-posterior effective stroke. A postoral band, the metatroch, parallels the prototroch and beats in opposition to it, with effective strokes from posterior to anterior. Particles small enough to fit between the prototroch and metatroch are captured between these two ciliary bands and transported to the mouth by a band of shorter cilia, the food groove. Particle capture by opposed bands has been described in larvae of two annelid families, the serpulids and the oweniids (Strathmann et al., 1972; Emlet and Strathmann, 1994), and larvae of several other families possess the ciliary bands necessary to feed in this way.

Another feeding mechanism known in annelid larvae involves active responses to individual food particles. For example, polynoid larvae lack an opposing metatroch and a ciliated food groove. These larvae swim forward until they encounter relatively large particles, then manipulate each particle individually into the mouth with a tuft of long compound cilia (Phillips and Pernet, 1996). Larvae belonging to related families (e.g., phyllodocids and nephtyids: Rouse and Fauchald, 1997) also lack a metatroch and a food groove (Bhaud and Cazaux, 1987), and are able to capture particles as large as bivalve larvae, but how they do this is not known. Additional feeding mechanisms are known or suspected from larvae of other annelid families (Strathmann, 1987; Nielsen, 1998).

The structural and functional variety of trochophores in annelids and related phyla has raised questions about their evolution (Strathmann, 1993; McHugh and Rouse, 1998). There is no consensus as to whether feeding or nonfeeding larvae are ancestral, or on which feeding mechanisms are primitive (Strathmann and Eernisse, 1994). Given uncertainties about such key issues as the distribution of traits among clades, the functional requirements for capturing particles, and the phylogeny of annelids, inferences about ancestral character states are weak.

Our study describes ciliation and mechanisms of particle capture in larvae of two families of annelids, the Opheliidae and the Echiuridae. We use these observations to compare the feeding capabilities of different annelid larvae and to suggest possible evolutionary transitions among annelid larval forms. These data also augment the number of informative characters available for phylogenetic inferences.

Hermans (1978) showed that larvae of the opheliid Armandia brevis possess prototrochal and metatrochal ciliary bands. Although the feeding mechanism was not described, these observations suggest that opposed-band feeding may occur. He also noted that late-stage A. brevis larvae are able to ingest large particles. A larva with 15 segments had ingested a tintinnid 80 [micro]m in diameter and a diatom 35 [micro]m in diameter and 260 [micro]m long (Hermans, 1964). This implies that these larvae were using a different feeding mechanism, since other work on annelid and mollusc larvae indicates that opposed-band feeding is limited to particles that fit between the prototroch and metatroch (typically spaced [less than]30 [micro]m apart: Strathmann et al., 1972; Strathmann and Leise, 1979).

Thus, limited observations suggested that A. brevis larvae might use several feeding mechanisms to capture particles of a broad range of sizes. Alternative mechanisms for the capture of larger particles by later stage larvae might supplement the opposed-band feeding mechanism. Such versatility might be particularly advantageous to later stage larvae if unfavorable allometric relationships reduce the profitability of opposed-band feeding as development progresses. An unfavorable allometry might occur if body volume and metabolic demands increase more rapidly than ciliary band area and maximum clearance rates as segments are added during development. Therefore, in addition to observing particle captures, we examined the relationship between clearance rates and body volume.

Echiurids have sometimes been placed in the phylum Annelida and sometimes in their own phylum, the Echiura, which is distinguished from the annelids by an apparent lack of segmentation (Nielsen, 1995). McHugh's (1997) molecular evidence shows that they are derived annelids, and she suggests that they should be placed in the annelid family Echiuridae. Larvae of the echiurid Urechis caupo bear prototrochal, metatrochal, and food-groove cilia (Newby, 1940; Suer, 1982), but how they capture particles has been unknown. We observed larval feeding in U. caupo to confirm use of the opposed-band feeding mechanism in the Echiuridae; to our surprise, we also obtained evidence that larger particles are captured at the mouth.

Our observations demonstrate that larvae in the annelid families Opheliidae and Echiuridae are able to capture particles both with opposed bands and directly at the mouth. This previously unrecognized combination of feeding mechanisms suggests hypotheses for evolutionary transitions among the diverse feeding larval forms of the Annelida.

Materials and Methods

Larval cultures

Reproductive adults of the opheliid Armandia brevis were collected in April and May 1998 in front of the Friday Harbor Laboratories, San Juan Island, Washington. Some animals were taken from beneath cobbles in the mid-inter-tidal zone and others from the plankton swarming at night to a light suspended from the laboratory dock. We isolated adults in finger bowls containing bag-filtered seawater (mesh size [less than or equal to] 10 [micro]m) until gametes were released. Eggs were fertilized by the addition of sperm and then rinsed with filtered seawater. Fertilized eggs were placed in 450-ml beakers that held filtered seawater and were partially submerged in a seawater table at 11[degrees]-13[degrees]C. Larvae were fed a mixture of the algae Isochrysis galbana and Chaetoceros gracilis.

Adults of the echiurid Urechis caupo were dug in inter-tidal mudflats in Bodega Harbor, California, in June of 1995 and held in aquaria at the Bodega Marine Laboratory for use throughout the summer. Methods described by Gould (1967) were used for obtaining gametes and fertilizing eggs. We reared larvae in 800-ml beakers cooled in aquaria at 10[degrees] to 16[degrees]C (median 13.3[degrees]C), approximately the temperature of the coastal seawater. The seawater was filtered through meshes of 30 or 70 [micro]m and larvae were fed the alga Rhodomonas sp. and occasionally Isochrysis galbana in addition to whatever food entered with the filtered seawater.

Ciliary bands

Light microscopy provided information about the ciliation of both opheliid and echiurid larvae. Larvae were viewed with differential interference contrast (DIC) optics for an optical section through the prototroch, food groove, and metatroch.

Scanning electron microscopy provided additional information about the ciliation of Armandia brevis. Larvae were relaxed in a 1:1 mixture of 7.5% [MgCl.sub.2] and seawater for 30 mm and fixed in 1% [OsO.sub.4] in seawater. After a rinse in seawater, fixed larvae were dehydrated in ethanol, infiltrated with hexamethyldisilazane for 30 min, and air-dried. They were mounted on stubs with double-sided tape and sputter-coated with gold-palladium before viewing.

Analysis of particle capture

To record larval feeding, we used video cameras mounted on compound and dissecting microscopes. A time-date generator indicated intervals between video images to the nearest 0.01 s. Larvae of Armandia brevis were presented with small and large particles in separate trials, and feeding activity was recorded at room temperature (22[degrees]C) onto VHS tape. We observed capture of small particles by placing several larvae on a slide with polystyrene-divinylbenzene spheres (Duke Scientific) of 5 and 12 [micro]m diameter (one size per slide), adding a raised coverslip, and viewing the larvae with a 20X objective and DIC optics. Larvae that had tethered themselves with mucous strands and were actively feeding (indicated by beating of both the prototroch and metatroch) were videotaped for about 10 min. We observed capture of large particles by placing larvae in a small petri dish onto a dissecting microscope and adding Sephadex beads ranging from 20 to 80 [micro]m in diameter. Larvae were videotaped as they swam an d fed.

For Urechis caupo larvae, feeding was observed at 15[degrees] to 20[degrees]C and recorded onto 8-mm tape. Larvae were confined within the spaces of a nylon mesh placed on a slide topped with a coverslip; they were free to rotate and change orientation but not to move forward continuously. We presented the larvae with three types of particles: the dinoflagellate Prorocenerum micans (length about 20 [micro]m), polystyrene-divinylbenzene spheres (diameter 5 to 29 [micro]m), and Sephadex beads (diameter 20 to 80 [micro]m).

The size of particles captured and ingested by U. caupo was analyzed by inspecting the gut contents of particle-fed larvae. Larvae and suspensions of particles of several sizes were placed in vials that were rotated at 15 rpm. After 5 min, the larvae were fixed with formaldehyde for gut-content examination.

Scaling of clearance rate and body volume

The relationship of maximum clearance rate to body volume was estimated for larvae of Armandia brevis with 6 to 16 setigerous segments. We counted the number of setigers and measured body length (for the entire larva), width (at the middle segment), and prototroch diameter of live larvae (n = 36) under a compound microscope with 4X objective. A video camera and image analysis program (NIH Image 1.61; available free at http://rsb.info.nih.gov/ nih-image) were used for these measurements. We estimated larval volume as a cylinder by the equation:

larval volume = [pi](D/2) [2] (L)

where D is body width and L is body length.

Maximum clearance rates were estimated as the volume of water passing through the prototroch per unit of time. To calculate these rates, we measured particle velocities and particle distances to the base of the prototroch from videotaped sequences of three larvae in each of three size classes (6-7, 11-12, and 15-16 setigers). We observed larvae and 5-[micro]m particles on a compound microscope with DIC optics and 20X objective lens, as described above. The larvae tethered themselves by mucous strands and were recorded for several minutes. The distances traveled by particles per unit of time and their distances to the base of the prototroch were measured from videorecorded sequences. Particles were measured as they passed within the direct influence of the cilia where velocities are negligibly affected by the slide or coverslip (Emlet, 1990).

We fitted binomial regressions from the origin through the plot of particle velocity versus particle distance from the cilium base. The rationale for fitting curvilinear lines to these data was both theoretical (Sleigh, 1984) and empirical (Strathmann and Leise, 1979). The studies in both areas suggest that velocity should increase from zero near the larval body surface to a maximum near the full length of the cilia; it should then decrease beyond the tips of the cilia. Since these curves included some particles that presumably passed beyond the tips of the cilia, it was necessary to estimate the lengths of the cilia for larvae of each of the three size classes. We measured cilium lengths (15 cilia per larva) with NIH Image from videotaped, live larvae with 0-17 setigers (n = 22 larvae). The binomial regression equations relating particle velocity to particle distance from the cilium base were then integrated from the origin (the base of the prototroch) to the estimated cilium length for that size class. The resulting areas represent estimates of the area of water that, in one unit of time, passes through one optical section of the prototroch in the plane of ciliary beat. We then estimated maximum clearance rates for each size class by multiplying that value by the circumference of the prototroch halfway between the base of the cilium and its tip (midpoint prototroch circumference). Finally, to determine whether maximum clearance rate scaled proportionately to body size during larval growth, we divided the maximum clearance rate for a given size class by the average body volume for that size class.

Results

Ciliary bands

Scanning electron micrographs clearly show the prototrochal and metatrochal cilia of Armandia brevis. The prototroch is made up of several rows of compound cilia that completely encircle the larval body anterior to the mouth (Fig. 1). The metatroch is a postoral band of compound cilia that extends laterally from the lower lip of the mouth around the larval body to a dorsal position (Fig. 1A). The metatrochal cilia on me lower lip are longer than the other metatrochal cilia (Fig. 1A, B). The prototroch and metatroch define the boundaries of a cilialined food groove. The width of the food groove lateral to the mouth was estimated from a scanning electron micrograph to be 10 [micro]m (SEM not shown). Dorsally, the food groove narrows. The mouth is large (about 50 [micro]m wide in the 18-setiger larva shown in Fig. 1B) and both its upper and lower surfaces are heavily ciliated (Fig. lA, B). A band of neurotrochal cilia runs along the ventral surface of the larva from just behind the mouth to the third setigerous segment (Fig. 1B).

Larvae of Urechis caupo also possess prototrochal and metatrochal ciliary bands (Fig. 2). The prototrochal cilia are longer than the metatrochal cilia. Again, these two ciliary bands define the boundaries of a food groove lined with simple cilia. Larvae also bear a midventral neurotroch, posterior to the mouth, and a telotroch.

Capture by opposed ciliary bands

In larvae of Armandia brevis and Urechis caupo, the movements of particles and the directions of recovery strokes of cilia indicated that the effective strokes of the prototrochal cilia were from anterior to posterior, and those of the metatrochal cilia were from posterior to anterior. For larvae of each species, we observed captures of more than 50 particles of 5 and 12 [micro]m in diameter; particles that came within reach of the prototroch were transported into the food groove between the prototroch and metatroch and moved to the mouth via the food groove, presumably by the food-groove cilia (Figs. 3-5). Particles were captured between prototroch and metatroch on the lateral and dorsal surfaces of the larva. Particles in the food groove moved around to the mouth from both the left and the right sides and both with and against the direction of rotation of the larval body. These particle paths indicate an opposed-band feeding mechanism.

Capture of large particles

Larvae of both species also captured particles at the mouth, without transport in the food groove. A late-stage larva of Armandia brevis (with[greater than] 14 setigers) captured two large particles (50 [micro]m in diameter) while videorecorded through a dissecting microscope (Fig. 6). When the swimming larva contacted a large particle in the vicinity of the mouth, the larva slowed and rotated so that the lower lip was aligned with the particle. The larva opened its mouth and ingested the particle, presumably using oral cilia or musculature.

Swimming Urechis caupo larvae used the mouth for direct capture of particles that passed over the episphere. Such captures occurred simultaneously with opposed-band particle captures (Fig. 5). Many of the particles caught directly by the mouth were too large to fit between opposed prototroch and metatroch, as illustrated by the gut contents in Figure 7 and the particles being rejected in Figure 8. In some cases the mouth gaped to admit a large particle. The 9-day-old larva in Figure 4 opened its mouth to a gape of about 35 [micro]m with a width of 95[micro]m. The 17-day-old larva in Figure 8 opened its mouth to 70 to 95 [micro]m, and the mouth's width when closed was about 125 [micro]m. Cilia on the mouth's lower lip (anterior to the shorter cilia of the neurotroch) appeared to aid the movement of large particles into the mouth. These cilia seemed to be continuous with the metatrochal band, which would account for the posterior-to-anterior current past these cilia. In some cases a particle was brought into t he mouth over the lower lip (Fig. 7).

Larvae of U. caupo captured large particles from an early stage. Small 4-day-old larvae ingested Sephadex spheres almost as large as those ingested by 16-day-old larvae (Table I). Even a 3-day-old larva ingested a 42-by-35-[micro]m mineral grain. Larger larvae did capture larger spheres, however. When early and later stage larvae were fed the same suspension, as in the last two lines of Table I, the median sizes and the largest sizes of ingested spheres were significantly greater for larger, older larvae (Mann-Whitney U tests, [n.sub.1] = 10, [n.sub.2] = 5, P [less than] 0.05). Objects larger than the spheres offered can be ingested. For example, a 49-day-old larva, 375 [micro]m wide, ingested an unidentified object 366 [micro]m long by 40 [micro]m wide.

When larvae of U. caupo of different ages and sizes were offered smaller plastic spheres, all 10 of the small, 3-day-old larvae caught fewer spheres of 29-[micro]m than of 12-[micro]m, and all 4 of the larger, 48-day-old larvae ingested more of the 29-[micro]m spheres than of the 12-[micro] spheres (Table II). Small, early-stage larvae did ingest 5- and 20-[micro]m spheres in about the same ratio as ingested by larger larvae (Table II). Estimates of the width of the food groove of a single 5-day-old larva ranged from 22 to 34 [micro]m, but the width of the food groove varies with contraction of the larva. The upper limit on the sizes of particles that could be transported in the food groove was not determined.

Rejection of particles

Larvae could actively reject particles. Particle rejection often occurred after a particle had been transported to the mouth and entered the esophagus. When a larva of Armandia brevis expelled a particle, the metatrochal cilia around the mouth stopped beating as the particle moved posteriorly down the body (Fig. 3). Metatrochal cilia at the mouth of larvae of Urechis caupo must also have altered beat during particle rejection, because large particles moved posteriorly over the lower lip and down the neurotroch during rejection (Fig. 8), in contrast to their posterior-to-anterior path over the lip during ingestion (Fig. 7).

For larvae of Armandia brevis, prototroch circumference and prototrochal cilium length increased with number of setigerous segments (Fig. 9A, B). Larval volume increased exponentially with number of setigers (Fig. 9C).

* Particle velocities increased slightly with number of setigers for larvae of A. brevis with 6-7, 11-12, and 15-16 setigers (n = 9) (Fig. 10). Increased particle velocities and cilium lengths resulted in a 30% increase in the area of water per prototrochal slice moved per second between larvae with 6-7 and 11-12 setigers and a 22% increase between larvae with 11-12 and 15-16 setigers (Table III). Maximum particle velocities were within the distal third of the cilium length (estimated for each size class from Fig. 9B), consistent with our expectations (Emlet and Strathmann, 1994). Although Strathmann et al. (1993) suggested that cilium lengths might be underestimated from videorecordings, our results indicate that this was not the case. In addition, our measurements agree with the cilium length of approximately 35 [micro]m reported by Hermans (1964) for a larva with an unspecified number of setigers.

Although estimated maximum clearance rates increased with number of setigers, they did not increase proportionately to body volume (Table III). Late-stage larvae (15-16 setigers) had a maximum ratio of clearance to body volume that was less than half of that achieved earlier in development (6-7 setigers; Table III).

Prototrochal circumference and cilium length both increased with larval growth to a greater extent for larvae of U. caupo than for larvae of A. brevis, over the stages measured (Tables I-III). The relative increase in body length was much less for U. caupo. Early-stage larvae were nearly spherical and elongated to the shape shown in Figure 2A at later stages. Data for particle velocities are lacking for U. caupo, but the increase in prototrochal area (cilium length times prototrochal circumference) relative to body volume was greater for this species than for A. brevis.

Discussion

Our observations add the Opheliidae and Echiuridae to those annelid families known to possess larvae with opposed-band feeding. As in other opposed-band feeders, larvae of both Armandia brevis and Urechis caupo possess a ciliated food groove between two parallel ciliary bands, a postoral metatroch and a prototroch. Direct observations confirm that particles are captured in the food groove (Figs. 3-5), probably through the combined action of long compound cilia in the prototroch (which beat anterior to posterior) and shorter compound cilia in the metatroch (which beat posterior to anterior). Simple cilia of the food groove may aid in retention of particles as well as in transport. This system is very effective in capturing relatively small particles (5-12 [micro]m), regardless of which part of the prototrochal circumference is contacted (ventral, lateral, or dorsal). How common this feeding method is in larvae of other opheliids or echiurids is not known, but larvae of at least one other echiurid bear opposed bands of cilia (Salensky, 1876; Hatschek, 1880).

Larvae of both A. brevis and U. caupo also ingested particles larger than the space between prototrochal and metatrochal bands. For A. brevis, it was later stage (14-17 setiger) larvae that ingested large (50-[micro]m) particles. These larvae approached large particles so that contact was directly at the mouth. This behavior was not observed in larvae at earlier stages. In contrast, larvae of U. caupo ingested particles greater than 50 [micro]m at early stages. Larvae of U. caupo did not appear to change orientation as they approached large particles; however, their movements were constrained by mesh cages. Particles that were captured directly at the mouth entered either over the episphere and prototroch or over the extension of the metatroch on the lower lip. In both species the mouths were large, could be opened to a wide gape, and were heavily ciliated. The cilia bordering the lower lip of the mouth appear to be a continuation of the metatroch. The oral cilia of A. brevis may include additional compound c ilia (Fig. 1). For both A. brevis and U. caupo, the large ciliated oral field and the large mouth aid in the capture of large particles.

The combination of two ciliary feeding mechanisms in individual larvae suggests hypotheses for evolutionary transitions among the feeding larvae of annelids. Some larvae, such as those of serpulids, appear to be restricted to capturing small particles between opposed bands; other larvae, like those of polynoids, lack opposed bands and appear to capture mostly large particles one by one, using complex oral ciliature (Phillips and Pernet, 1996). Our results demonstrate that in at least two families of annelids, both types of mechanisms can be employed simultaneously by the same larva. In addition, it appears that the oral ciliature of A. brevis and U. caupo, which is responsible for the capture of large particles, is continuous with the lateral and dorsal extensions of the metatroch and food groove. As an evolutionary transition, expansion of oral ciliation might result in a food groove and metatroch paralleling the whole length of the prototroch to produce an opposed-band system. Alternatively, enlargement of the mouth and elaboration of oral ciliation (with loss of the lateral and dorsal parts of the opposed-band system) could produce the variety of oral ciliature found in the diverse feeding larvae of annelids. Continued modification of such cilia might result in such unusual and functionally important structures as the group of long compound cilia on the left side of the mouth of polynoid larvae.

Estimated maximum clearance rates did not scale isometrically with body volume among the three size classes of A. brevis. Cilium length, prototroch circumference, and particle velocities through a prototrochal slice all increased as body volume increased, but not enough for maximum clearance rate to increase in proportion to body volume--thus the volume of water swept by cilia decreases relative to body volume as the larva adds segments. An analogous situation has been described for the cyphonautes larva of bryozoans, in which ciliated band length does not increase proportionately to body volume during growth and development (McEdward and Strathmann, 1987). This allometry is potentially unfavorable to larger larvae. In asteroid, echinoid, and bivalve larvae similar in size to A. brevis larvae, metabolic rates scale isometrically with body mass (HoeghGuldberg and Manahan, 1995). Further, in the larvae of an echinoid, metabolic demand scales isometrically with larval volume (McEdward, 1984). If these results c an be generalized to larvae of A. brevis, and if we make the reasonable assumption that the masses of these larvae are proportional to their volume, then the maximum clearance rates of A. brevis larvae decline relative to metabolic demand as the larvae increase in size. However, larger larvae of A. brevis ([greater than]12 setigers) can supplement the amount of small particles captured by opposed-band feeding by capturing larger particles at the mouth. The increased size range of food may compensate, at least partly, for the decrease in clearance rate. This decrease in maximum clearance rate per larval volume may have selected for larvae that possess two types of feeding mechanisms.

Do other annelid larvae share this potentially unfavorable allometry of maximum clearance rate and body volume? Some annelid larvae resemble A. brevis in extreme elongation of a segmented body during the larval stage (Bhaud and Cazaux, 1987). Some of these larvae (e.g., spionids) possess feeding mechanisms other than the opposed prototrochal and metatrochal bands. Thus, evolutionary changes in the size range of particles captured may have been favored in several groups of annelids as a result of a small head circumference and long larval body. Other possible solutions to this problem are opposed bands elongated on ciliated lobes, as reported for the rostraria larva of an annelid (Jagersten, 1972), or the sinuous opposed bands of mitraria larvae of oweniid annelids (Emlet and Strathmann, 1994).

The larvae of U. caupo and some other annelids probably do not face such an unfavorable allometry of maximum clearance rate to body volume, however. The larvae of U. caupo develop from nearly spherical trochophores (at 3 to 5 days) to forms with more elongate bodies (at several weeks), but the elongation is not as extreme (cf. Fig. 2 to Fig. 6). Also, these larvae capture relatively large particles from an early stage. Nevertheless, the circumferential ciliary bands are shorter, relative to body size, than similar bands that are extended on the velar lobes of many gastropod larvae (Richter and Thorson, 1975). Feeding on an extended size range of particles and extension of opposed, ciliary bands on lobes may be alternative ways of increasing ingestion rates.

Further analyses of larval feeding methods, as well as robust phylogenies, are required to understand the evolution and functional consequences of diverse larval feeding mechanisms in the Annelida. For example, why are opposed bands apparently used only in the capture of small particles? What functional constraints place an upper limit on the spacing of the prototroch and metatroch in opposed-band feeders? Such analyses may also reveal why some larvae (e.g., serpulids) use restricted opposed bands to feed on small particles, and others (e.g., polynoids) use complex oral ciliature to feed primarily on large particles instead of employing both methods, as do the opheliid and echiurid larvae described here.

Acknowledgments

NSF grant OCE9633193, the Robert Fernald Fellowship endowment, and the Friday Harbor Laboratories of the University of Washington supported the research on Armandia brevis. NSF grant OCE9301665 and the Bodega Marine Laboratory of the University of California at Davis supported the research on Urechis caupo. K. Uhlinger advised on collection of adults and culture of larvae of U. caupo. W. Borgeson provided algal medium and Isochrysis galbana. N. E. Phillips and C. Staude advised on analysis of videotapes of U. caupo. We thank J. Marcus for help in printing photographs, and J. Hoffman and two anonymous reviewers for useful comments on the manuscript.

(1.) Department of Zoology, University of Florida, 223 Bartram Hall, Gainesville, Florida 32611;

(2.) Department of Zoology, Cordley Hall 3029, Oregon State University, Corvallis, Oregon 97331;

(3.) Friday Harbor Laboratories and Department of Zoology, University of Washington, 620 University Road, Friday Harbor, Washington 98250;

(4.) Department of Biology and Oregon Institute of Marine Biology, University of Oregon, P.O. Box 5389, Charleston, Oregon 97420

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               Sizes of Sephadex spheres ingested by larvae
                of Urechis caupo differing in size and age
                                           Particle diameter
                                            ([micro]m) [+]
 Age   Prototrochal diameter Cilium length
(days)    ([micro]m) [*]      ([micro]m)     In suspension      Ingested
  4             159               45        45, 26-73 (50)   36, 19-53 (51)
  5             165               44        44, 30-74 (50)   36, 19-60 (34)
 16             318               65        44, 30-74 (50)   38, 21-73 (104)
 Age    Number
(days) of larvae
  4       12
  5       10
 16        5
(*.)Diameter of the prototrochal band is
diameter at the base of the prototrochal cilia.
(+.)Values are median, range, and (in
parentheses) number of particles.
                Sizes of plastic spheres ingested by larvae
                of Urechis caupo differing in size and age
                                            Particle diameter
 Age   Prototrochal diameter Cilium length Ratio in suspension
(days)    ([micro]m) [*]      ([micro]m)    (29:12 [micro]m)
  3             151               46             1.43:1
 48             347               76             1.43:1
                                             (20:5 [micro]m)
  4             161               45               1:1
 15             310               67               1:1
 Age    Ratio ingested   Number
(days) (29:12 [micro]m) of larvae
  3     39/146 = 0.27      10
 48     206/112 = 1.84      4
       (20:5 [micro]m)
  4      146/30 = 4.9       8
 15      99/37 = 2.7        8
(*.)Diameter of the prototrochal band is
diameter at the base of the prototrochal cilia.
          Estimated clearance rate and clearance rate per larval
        volume for three size classes of larvae of Armandia brevis
           Cilium                   Water area per
  # of     length                  prototroch slice
Setigers ([micro]m) [*] per unit time [+] ([micro][m.sup.2]/s)
  6-7       29.9                        32846
 11-12      34.8                        42602
 15-16      36.4                        51949
                 Midpoint
  # of         prototrochal             Max. clearance rate
Setigers circumference ([micro]m) ([micro][m.sup.3]/s)X[10.sup.6]
  6-7              422                         13.9
 11-12             549                         23.4
 15-16             642                         33.4
               Larval             Clearance
  # of         volume            rate/volume
Setigers ([micro][m.sup.3]) [++]    (1/s)
  6-7          998309               13.9
 11-12        2526475                9.3
 15-16        5310250                6.3
(*.)Calculated from the binomial regression in Fig. 10B.
(+.)Calculated from the areas under the curves in Fig. 11, bound
by the origin and the estimated cilium length for that size class.
(++.)Estimated from the binomial regression in Fig. 10C.
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Author:MINER, BENJAMIN G.; SANFORD, ERIC; STRATHMANN, RICHARD R.; PERNET, BRUNO; EMLET, RICHARD B.
Publication:The Biological Bulletin
Geographic Code:1USA
Date:Aug 1, 1999
Words:5950
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