Body Form and Patterns of Ciliation in Nonfeeding Larvae of Echinoderms: Functional Solutions to Swimming in the Plankton?

SYNOPSIS. Nonfeeding larval forms of echinoderms are believedto have evolved repeatedly from feeding larval forms, and thesetransformations usually result in major shifts in morphogenesis.Current hypotheses on form change invoke relaxation of stabilizingselection on traits that functionin feeding, coupled with selectionfor rapid development of juvenile traits. However, comparativeevidence from 51 species of nonfeeding larvae, representing19 independent origins, suggests that body form, patterns ofciliation, and possibly buoyancy reflect functional requirementsfor maintenance of swimming performance. Nonfeeding larvae withbody lengths less than 600 µm usually have several transverseciliated bands, while those with body lengths greater than 800µm usually have uniform ciliation. A preliminary modelwhich compares estimated drag and buoyancy forces with ciliarypropulsive forces predicts that bands of simple cilia do notproduce sufficient propulsive forces to permit swimming in largerlarvae. For larger larvae, increases in areal coverage of ciliamay be required to produce propulsive forces sufficient to opposedrag and buoyancy forces and permit movement. For these largerlarvae, estimates of water velocities at the tips of uniformarrays of cilia are well below the upper limits of water movementsby cilia of echinoderms. Functional constraints on nonfeedinglarval forms should be considered, along with (above mentioned)current hypotheses, in explanations of morphogenetic changesassociated with transition from feeding to nonfeeding larvaldevelopment.     

The nonfeeding auricularia of Holothuria mexicana (Echinodermata,Holothuroidea)

Among echinoderms, nonfeeding larvae usually are simplified in body shape, have uniform ciliation, and have lost the larval gut. A few species have nonfeeding larvae that express some remnant features of feeding larvae like ciliated bands and larval skeleton or larval arms, but typically their larval mouth never opens and their gut does not function. Still other species have retained the feeding larval form, a functional gut, and can feed, but they do not require food to metamorphose. The present note describes the development of a tropical holothurian, Holothuria mexicana, which hatches as a gastrula that is already generating coelomic structures. A translucent auricularia forms with a mouth that opens but becomes reduced soon thereafter. In form and ciliation this auricularia resembles a feeding larva, but it does not respond to food. A doliolaria forms on day 4 and the pentactula on day 6 post‐fertilization. Further study of this larva and that of its closely related congener, Holothuria floridana, is warranted.     

The morphology of cilia in sponge larvae

Sponge larvae possess cilia with unusual terminal expansions which are curled or biconcave in shape externally, as seen by scanning electron microscopy. Thin sections, passing through the point where the ciliary shaft enters the expanded area reveal the ciliary axoneme to be surrounded by many membranous folds, some of which are vesicular. The ‘club footed’ cilia occur in disparate groups of Demospongiae and most frequently, all larval cilia are of this type. There is no immediately obvious correlation between the type of movement displayed by the larvae and the occurrence of terminally expanded cilia.     

Ciliary sieving and active ciliary response in capture of particles by suspension-feeding brachiopod larvae

Larvae of a brachiopod, Glottidia pyramidata, used at least two ciliary mechanisms to capture algal cells upstream from the lateral band of cilia that produces a feeding/swimming current. (1) Filtration: the larvae retained algal cells on the upstream (frontal) side of a sieve composed of a row of stationary laterofrontal cilia. Movement of the laterofrontal cilia could not be observed during capture or rejection of particles, but the laterofrontal cilia can bend toward the beating lateral cilia, a possible mechanism for releasing rejected particles from the ciliary sieve. (2) Localized changes of ciliary beat: the larvae may also concentrate particles by a local change in beat of lateral cilia in response to particles. The evidence is that the beat of lateral cilia changed coincident with captures of algal cells and that captured particles moved on paths consistent with a current redirected toward the frontal side of the tentacle by an induced local reversal of the lateral cilia. The change of beat of lateral cilia could have been an arrest rather than a reversal of ciliary beat, however. The similar ciliary bands in adult and larval lophophorates (brachiopods, phoronids, and bryozoans) suggest that these animals share a range of ciliary behaviours. The divergent accounts of ciliary feeding of lophophorates could be mostly the result of different authors observing different aspects of ciliary feeding.     

Opposed bands of cilia in the nonfeeding larvae of the serpulid annelid Salmacina tribranchiata

The nonfeeding planktonic larvae of marine invertebrates typically lack larval feeding structures. One puzzling exception to this generalization is the annelid clade Sabellidae, in which nonfeeding larvae possess ciliary bands (specifically, food groove and metatroch) that, to the best of our knowledge, have no function other than in feeding. Nishi and Yamasu (1992b, Bulletin of the College of Sciences, University of the Ryukyus, 54 , 107–121) published a scanning electron micrograph showing that nonfeeding larvae of the serpulid annelid Salmacina dysteri also possess food groove and metatrochal cilia. Here I demonstrate that nonfeeding larvae of Salmacina tribranchiata also bear ciliary bands identifiable as food groove and metatroch by position. High‐speed video of ciliary beat patterns shows that, together with the prototrochal cilia, these bands function in an opposed band system. The presence of feeding structures in nonfeeding annelid larvae is thus more widely distributed than previously recognized. The presence of feeding structures may make evolutionary transitions to planktotrophy more likely, and may underlie an inferred origin of larval feeding in the common ancestor of one of the two major clades of serpulid annelids, Serpulinae.     

The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae

Despite the embryological and anatomical disparities present among lophotrochozoan phyla, there are morphological similarities in the cellular arrangements of ciliated cells used for propulsion among the nonfeeding larval forms of kamptozoans, nemerteans, annelids, mollusks, and bryozoans. Evaluating whether these similarities are the result of convergent selective pressures or a shared (deep) evolutionary history is hindered by the paucity of detailed cellular information from multiple systematic groups from lesser-known, and perhaps, basal evolutionary phyla such as the Bryozoa. Here, I compare the ciliary fields and musculature among the major morphological grades of marine bryozoan larvae using light microscopy, SEM, and confocal imaging techniques. Sampling effort focused on six species from systematic groups with few published accounts, but an additional four well-known species were also reevaluated. Review of the main larval types among species of bryozoans and these new data show that, within select systematic groups of marine bryozoans, there is some conservation of the cellular arrangement of ciliary fields and larval musculature. However, there is much more morphological diversity in these structures than previously documented, especially among nonfeeding ctenostome larval types. This structural and functional diversification reflects species differences in the orientation of the apical disc during swimming and crawling behaviors, modification of the presumptive juvenile tissues, elongation of larval forms in the aboral-oral axis, maximizing the surface area of cell types with propulsive cilia, and the simplification of ciliary fields and musculature within particular lineages due to evolutionary loss. Considering the embryological origins and functional plasticity of ciliated cells within bryozoan larvae, it is probable that the morphological similarities shared between the coronal cells of bryozoan larvae and the prototrochal cells of trochozoans are the result of convergent functional solutions to swimming in the plankton. However, this does not rule out cell specification pathways shared by more closely related spiralian phyla. Overall, among the morphological grades of larval bryozoans, the structural variation and arrangement of the main cell groups responsible for ciliary propulsion have been evolutionarily decoupled from the more divergent modifications of larval musculature. The structure of larval ciliary fields reflects the functional demands of swimming and substrate exploration behaviors before metamorphosis, but this is in contrast to the morphology of larval musculature and presumptive juvenile tissues that are linked to macroevolutionary differences in morphogenetic movements during metamorphosis.     

Development of the Nervous System of Sea Urchin Embryos: Formation of Ciliary Bands and the Appearance of Two Types of Ectoneural Cells in the Pluteus

An ultrastructural study of the larval integument of the sea urchin, Hemicentrotus pulcherrimus , was conducted with special emphasis on the development of the nervous system in relation to the formation of ciliary bands. In the integument of 4-armed pluteus larvae, cells associated with the ciliary band, which have 200 nm-thick projections at their apices, and cells in the squamous epithelium, which have a cilium and long, fine radiating processes in the apical region, were observed. Both cell types have axons at their basal ends that form nerve bundles beneath the ciliary bands, where the axons make contact with ectodermal effector cells with motile cilia. The cilia and other apical projections of these ectoneural cells run parallel to the surface of the cells, and are under the hyaline layer. The axoneme of the cilium has a typical "9 + 2" microtubular arrangement, but generally has no dynein arms. These ectoneural cells are more frequent on the oral surface than on the antioral surface.     

Ciliary filter-feeding structures in adult and larval gymnolaemate bryozoans

Abstract. Ciliary filter-feeding structures of gymnolaemate bryozoans—adults of Flustrellidra hispida and Alcyonidium gelatinosum , larvae of Membranipora sp.—were studied with SEM. In F. hispida and A. gelatinosum , the distal part of each tentacle has a straight row of stiff laterofrontal cilia which carry out "ciliary sieving" to capture suspended food particles that are subsequently transported downward towards the mouth by tentacle flicking; both structure and function resemble those of stenolaemate tentacles. The proximal part of the tentacle and of the ciliary ridge of a cyphonautes larva have strikingly similar structures, except that the laterofrontal cells are monociliate in the adults and biciliate in the larvae. The laterofrontal cells of the tentacles are arranged in a zigzag row and their cilia form two parallel rows, a frontal and a lateral row. The latter probably forms the sieve of stiff filter cilia in front of the water-pumping lateral cilia, whereas the frontal row appears to be held close to the frontal ciliary band of the tentacle. The biciliate laterofrontal cells of the cyphonautes larva have the cilia arranged in similar rows. The detailed morphological similarities between the ciliary bands of adult and larval filtering structures suggest that the feeding mechanisms are similar, contrary to what has been previously thought.     

Cilia formation in the adult cat brain after pargyline treatment

The brains of four adult cats treated with pargyline (a nonhydrazide monoaminoxidase inhibitor) were examined at both the light and electron microscopic levels. Formation of typical mature cilia with the 9 + 2 pattern was observed in neural cells in the following areas: habenula nuclei, interpeduncular nuclei, hippocampus, mammillary bodies, thalamus, and caudate nucleus. The most marked ciliation occurs in the habenula nuclei. In general, glial cells greatly predominate in the formation of cilia. It is not clear whether ciliation in the central nervous system is the direct result of pargyline or if it occurs indirectly as a result of inhibition of monoaminoxidase. These findings are compared with the serotonin effect on ciliation in the embryogenesis of lower forms. It is suggested that pharmacological stimulation of centriolar reproduction without subsequent mitosis may lead to ciliary formation.     

Contrasting scaling of ciliary filters in swimming larvae and sessile adults of fan worms (Annelida: Polychaeta)

Abstract. Both larval and adult fan worms capture particles with opposed bands of cilia. While the larvae use one of the opposed bands (the prototroch) for both feeding and swimming, the sessile adults rely partly on ambient currents to bring food particles to the ciliary bands. The scaling of length of prototrochal cilia with larval body size contrasts with scaling of the opposed latero-frontal cilia with adult body size. In the larva of the serpulid Hydroides elegans , the length of prototrochal cilia increased from 28 to 42 μm in early to late-stage larvae. In contrast, latero-frontal cilia did not increase in length (23 μm) during postlarval development of H. elegans. Among adults of 5 fan-worm species, lengths of latero-frontal cilia ranged from 22 to 35 μm and were weakly correlated with body size. The total area of ciliary filter nevertheless increased with increasing body dry weight of worms with an allometric exponent similar to exponents reported for gill and lophophore areas vs. body weight within species of suspension-feeding bivalves, brachiopods, and gastropods. The similar scaling was remarkable given the striking differences in distribution and function of the ciliary filters. In adult fan worms, increases in filter area depended largely on increases in number and length of radioles; differences in branching of radioles had little effect. Radioles were commonly in 2 or more rows in series, implying refiltration in still water by downstream radioles. Since the allometry of worms' filter area with body size depends on filters in series, it depends on ambient currents that overwhelm ciliary currents.     

Opposed ciliary bands in the feeding larvae of sabellariid annelids

The larvae of marine annelids capture food using an unusual diversity of suspension-feeding mechanisms. Many of the feeding mechanisms of larval annelids are poorly known despite the abundance and ecological significance of both larvae and adults of some annelid taxa. Here we show that larvae of two species of sabellariid annelids, Sabellaria cementarium and Phragmatopoma californica, bear prototrochal and metatrochal cilia that beat in opposition to each other. For larvae of S. cementarium, we provide evidence that these opposed bands of cilia are used to capture suspended particles. In video recordings, captured particles were overtaken by a prototrochal cilium and then moved with the cilium to the food groove, a band of cilia between the prototroch and metatroch. They were then transported by cilia of the food groove to the mouth. Lengths of the prototrochal cilia, lengths of the prototrochal ciliary band, size range of the particles captured, and estimated rates of clearance increased with larval age and body size. Confirmation of the presence of opposed bands in larvae of sabellariids extends their known occurrence in the annelids to members of 10 families. Opposed bands in these different taxa differ in the arrangements and spacing of prototrochal and metatrochal cilia, and in whether they are used in combination with other feeding mechanisms. Opposed bands appear to be particularly widespread among the larvae of sabellidan annelids (a clade that includes sabellariids, sabellids, and serpulids), even in some species whose larvae do not feed. A parsimony analysis suggests that opposed bands are ancestral in this clade of annelids.     

Good eaters, poor swimmers: compromises in larval form

Compromises between swimming and feeding affect larval formand behavior. Two hypotheses, with supporting examples, illustratethese feeding-swimming trade-offs. (1) Extension of ciliatedbands into long loops increases maximum clearance rates in feedingbut can decrease stability of swimming in shear flows. A hydromechanicalmodel of swimming by ciliated bands on arms indicates that morphologieswith high performance in swimming speed and weight-carryingability in still water differ from morphologies conferring highstability to external disturbances such as shear flows. Instabilityincludes movement across flow lines from upwelling to downwellingwater in vertical shear. Thus a hypothesis for the high armelevation angles of sea urchin larvae, which reduce speed instill water, is that they reduce a downward bias imposed bythe vertical shear in turbulence. Observations of sea urchinlarvae in vertical shear and comparisons among brittle starlarvae are consistent with the performance trade-offs predictedby the model. (2) Structures and behaviors that reduce swimmingspeed can enhance filtering for feeding. In the opposed-bandfeeding mechanisms of veligers and many trochophores, ciliapush water to swim but movement of cilia relative to the wateroccurs when cilia overtake and capture particles. Features thatmay increase clearance rates at the expense of speed and weightcapacity include structures that increase drag or body weightand a ciliary band that beats in opposition to the feeding-swimmingcurrent. Larval feeding mechanisms inherited from distant ancestorsresult in different swimming-feeding trade-offs. The differenttrade-offs further diversify larval form and behavior.     

Versatile ciliary behaviour in capture of particles by the bryozoan cyphonautes larva

Cyphonautes larvae of a bryozoan, Membranipora membranacea, used several ciliary mechanisms to capture algal cells upstream from the lateral band of cilia that produces a feeding current. (1) Lateral cilia changed beat and a backcurrent occurred at the time and place that particles were retained. (2) Algal cells were sieved and held stationary at the upstream (frontal) side of a row of laterofrontal cilia that were not beating. (3) Localized extension of cilia toward the inhalant chamber, coincident with particle captures, indicated that laterofrontal cilia flick toward the inhalant chamber. These flicks may aid transport of captured particles toward the mouth. Thus my earlier report that larvae only sieve, in contrast to the adults (which have an active ciliary response) was in error. The similar ciliary bands in adult and larval bryozoans and in other lophophorates (brachiopods, and phoronids) suggest that these animals share a core repertoire of ciliary behaviours in the capture and concentration of suspended food particles.     

A Distinctive Nerve Cell Type Common to Diverse Deuterostome Larvae: Comparative Data from Echinoderms,Hemichordates and Amphioxus

Abstract The larval ciliary bands of echinoderm bipinnaria and pluteus larvae and the hemichordate tornaria contain similar multipolar or bipolar nerve cells with unusual apical processes that run across the surface of the band between the bases of its cilia. We report on some distinctive ultrastructural features of these cells. Among these are specialized junctions that occur between the cells' apical processes and adjacent ciliary band cells near the base of each cilium. Such structures are best developed in pluteus larvae. Many nerve cells in the larval spinal cord of amphioxus also have large apical processes that cross the central lumen of the cord. We interpret our observations on these cells in terms of Garstang's hypothesis, which derives the chordate neural tube from a larval ciliary band, and suggest that multipolar cells like those in echinoderm and tornaria bands may be the antecedents of some categories of neurons in the chordate spinal cord.     

Swimming Speed of Larval Snail Does Not Correlate with Size and Ciliary Beat Frequency

Many marine invertebrates have planktonic larvae with cilia used for both propulsion and capturing of food particles. Hence, changes in ciliary activity have implications for larval nutrition and ability to navigate the water column, which in turn affect survival and dispersal. Using high-speed high-resolution microvideography, we examined the relationship between swimming speed, velar arrangements, and ciliary beat frequency of freely swimming veliger larvae of the gastropod Crepidula fornicata over the course of larval development. Average swimming speed was greatest 6 days post hatching, suggesting a reduction in swimming speed towards settlement. At a given age, veliger larvae have highly variable speeds (0.8–4 body lengths s⁻¹) that are independent of shell size. Contrary to the hypothesis that an increase in ciliary beat frequency increases work done, and therefore speed, there was no significant correlation between swimming speed and ciliary beat frequency. Instead, there are significant correlations between swimming speed and visible area of the velar lobe, and distance between centroids of velum and larval shell. These observations suggest an alternative hypothesis that, instead of modifying ciliary beat frequency, larval C. fornicata modify swimming through adjustment of velum extension or orientation. The ability to adjust velum position could influence particle capture efficiency and fluid disturbance and help promote survival in the plankton.     

The evolution of land plant cilia

Eukaryotic cilia/flagella are ancient organelles with motility and sensory functions. Cilia display significant ultrastructural conservation where present across the eukaryotic phylogeny; however, diversity in ciliary biology exists and the ability to produce cilia has been lost independently on a number of occasions. Land plants provide an excellent system for the investigation of cilia evolution and loss across a broad phylogeny, because early divergent land plant lineages produce cilia, whereas most seed plants do not. This review highlights the differences in cilia form and function across land plants and discusses how recent advances in genomics are providing novel insights into the evolutionary trajectory of ciliary proteins. We propose a renewed effort to adopt ciliated land plants as models to investigate the mechanisms underpinning complex ciliary processes, such as number control, the coordination of basal body placement and the regulation of beat patterns.     

Ciliated band structure in planktotrophic and lecithotrophic larvae of Heliocidaris species (Echinodermata: Echinoidea): a demonstration of conservation and change

The evolution of lecithotrophic (non-feeding) development in sea urchins is associated with reduction or loss of structures found in the planktotrophic (feeding) echinopluteus larvae. Reductions or losses of larval feeding structures include pluteal arms, their supporting skeleton and the ciliated band that borders them. The barrel-shaped lecithotrophic larva of Heliocidaris erythrogramma has, at its posterior end, two or three ciliated band segments comprised of densely packed, elongate cilia. These cilia may be expressions of the epaulettes that would have been present in an ancestral larval form, represented today by the feeding echinopluteus of H. tuberculata . We compared the development and cellular organization of the larval ciliary structures of both Heliocidaris species to assess whether the ciliary bands of H. erythrogramma are expressions of the feeding ciliated band or epaulettes of an echinopluteus. Epaulette development in feeding larvae of H. tuberculata involves separation of specific parts of the ciliated band from the rest of the feeding ciliated band, hyperplastic addition of ciliated cells and hypertrophic growth of the cilia. Like epaulettes, the ciliated bands of H. erythrogramma are composed of long spindle-shaped cells arranged in a cup-shaped collection that bulges into the blastocoel; and these cells have elongated cilia. In their developmental origin and topological arrangement however, the ciliated bands of H. erythrogramma correspond more closely with parts of the pluteal feeding ciliated band than with epaulettes. The larvae of this echinoid appear to develop epaulette-like bands from parts of the original (but reduced) feeding ciliated band. The evolution of development in H. erythrogramma has thus involved both conservation and change in echinopluteal ciliary structures.     

LiCl inhibits the establishment of left-right asymmetry in larvae of the direct-developing echinoid Peronella japonica

The effect of LiCl on the establishment of left-right (LR) asymmetry in larvae of the direct-developing echinoid Peronella japonica was investigated with special attention to the location of the amniotic opening and ciliary band pattern. The larvae of echinoids are LR symmetric, but shortly before metamorphosis the larval LR symmetry is lost as a result of the formation of an amniotic cavity (vestibule), part of the adult rudiment, on the left side of the body. P. japonica has been considered to be the only exception among the echinoids, because the amniotic cavity forms at the midline of the larval body. In the present study we discovered the following two different LR asymmetric traits in larvae of P. japonica: the opening of the amniotic cavity initially forms at the midline of the larval body but shifts to the left dorsal side, and a looped ciliary band that initially forms with LR symmetry becomes LR asymmetric as a result of the formation of a bulge on left dorsal side. The establishment of LR asymmetry in both the location of the amniotic opening and the change in the shape of the ciliary band was influenced by exposing embryos to LiCl. Quantitative analysis of the shift in amniotic opening showed that exposure of embryos to LiCl causes repression of leftward shifting of the amniotic opening in earlier stage larvae, and leftward or rightward shifting in later stage larvae. These findings suggest that LiCl is an effective means of impairing the establishment of LR asymmetry in sea urchin embryos.     

Effects of cryopreservation on the ultrastructural anatomy of 3-segment Nereis virens larvae (Polychaeta)

Abstract. A transmission electron microscope study of fresh and cryopreserved Nereis virens larvae at the three chaetiger stage is described with special emphasis on examining the structure of the photoreceptors and surface ciliation of the head, the midgut epithelium, and muscle cells. Complex ectodermal structures such as the developing rhabdomeric adult eyes were unaffected by the cryopreservation procedure. Some loss of surface cilia on the prostomium was observed but is not life-threatening though it may restrict ciliary swimming in the recovered larvae. Loss of pigment from the prostomium is caused by osmotic stress. Structural damage was observed in the digestive tissues of the larvae cryopreserved before or after the optimum stage of development. This damage is potentially more serious and may account for the relatively short time period during development where cryopreservation can be successfully applied.