Development and differentiation of the eye in Platynereis dumerilii (Annelida,Polychaeta)

The nereid polychaete, Platynereis dumerilii, possess two pairs of post-trochophoral eyes with one vitreous body each. The development of these eyes has first been observed in 2-day-old larvae. Whether the eye anlagen arise from stem cells or from undifferentiated ectodermal tissue was not determined. At first, the anlagen of the anterior and the posterior eyes adjoin each other. They separate in late 3-day-old larvae. The first separated eye complexes consist each of two supporting and two sensory cells. The supporting cells synthesize two different kinds of granules, the pigment granules of the pigment cup and the prospective tubules of the vitreous body. These tubules accumulate in the distal process of the supporting cell. The vitreous body is formed by compartments of the supporting cells filled with the osmiophilic vitreous body tubules. The short, bulbar photosensory processes bear microvilli that emerge into the ocular cavity. At the apex of each sensory cell process, a single cilium (or occasionally two) arises. The sensory cells contain a different kind of pigment granule within their necks at the level of the pigment cup. The rate of eye development and differentiation varies. New supporting cells are added to the rim of the eye cup. They contribute to the periphery of the vitreous body like onion skins, and sensory cells move between supporting cells. The older the individual compartments of the vitreous body are, the more densely packed is their content of vitreous body tubules. Elongation of the sensory and supporting cell processes of the older cells increases the volume of the eye. The eyespots of the trochophore are briefly described as of the two-celled rhabdomeric type with a single basal body with ciliary rootlet.     

Central nervous system and sense organs, with special reference to photoreceptor-like sensory elements, in Polygordius appendiculatus (Annelida), an interstitial polychaete with uncertain phylogenetic affinities

Abstract. The phylogenetic position of Polygordius is still pending; relationships with either Opheliidae or with Saccocirrus are the most favored hypotheses. The present study of Polygordius appendiculatus was designed to look for morphological characters supporting either of these two hypotheses. The homology of the anterior appendages, and the structure of the central nervous system and nuchal organ all required clarification; we also examined whether photoreceptor‐like sense organs exist in adults. From their innervation pattern, it is likely that the anterior appendages represent palps. They lack structures typical of palps in Canalipalpata, such as musculature and coelomic cavities, which would be expected in the case of a saccocirrid relationship. Thirteen photoreceptor‐like sense organs were found in front of the brain, the only structures resembling photoreceptors in adults of P. appendiculatus. These multicellular sense organs comprise a supportive cell and several sensory cells enclosing an extracellular cavity. There are three different types of sensory cells: one rhabdomeric and two ciliary. These sensory cells are combined differently into three forms of sense organ: the most frequent uses all three types of sensory cells, the second possesses one rhabdomeric and one ciliary cell type, and the third has two types of ciliary sensory cells. Whereas similar sensory cells are frequently found in various polychaetes, their combination in one sensory organ is unique to Polygordius and is considered to represent an autapomorphy. The nuchal organs exhibit features typical of polychaetes; there are no specific features in common with Saccocirrus. Instead, the covering structures show obvious similarities to Opheliidae, as can also be found in the central nervous system. Altogether, the current observations do not contradict a relationship with opheliids but provide no evidence of a relationship with Saccocirrus as has been found in certain molecular analyses, and thus currently leave the phylogenetic position of Polygordius unresolved.     

Giant pelagic larvae of Phyllodocidae (Polychaeta,Annelida)

The microscopic anatomy of giant pelagic larvae of Phyllodocidae was studied using routine histological, SEM, and TEM techniques. The larvae consist of two distinct regions: a large spherical trochophore measuring up to 2 mm in diameter and a posterior, long (up to 10 mm length), narrow rudiment of the adult body with up to 120 segments. The larvae have an unusual mixture of larval and adult features, including a very complex, well-developed brain and ganglia in the ventral nerve cord, and only a single pair of protonephridia located in the hyposphere of the trochophore. A muscular pharynx is not developed. The intestinal wall, especially in the trochophore region, consists of endodermal cells containing considerable nutritive material in the form of yolk-like globular inclusions. The digestive tract of all larvae was empty. The position of the frontal sensory organ and the prototroch, the structure of the parapodia and setae, and the three pairs of tentacular cirri dictate inclusion of the larvae in the family Phyllodocidae. The relatively enormous size and unusual pattern of development of the adult body may be adaptations for a long pelagic life and rapid settlement of the species, which inhabits slopes of islands and underwater mounts located far apart. J. Morphol. 238:93–107, 1998. © 1998 Wiley-Liss, Inc.     

Presumptive photoreceptor structures of the trochophore of Harmothoë imbricata (Polychaeta)

The behaviour of the Harmothoë trochophore changes with age, the larva being phototropic initially and later photonegative.

The trochophore possesses two ocelli midway between the prototroch and the apex in a mid‐lateral position. They appear first at the eighth day of development and grow to be kidney‐shaped structures. There is a pigment cup derived from a single cell that encloses a rhabdomeric type of photoreceptor apparatus that is also derived from a single (or rarely two) cell.

In the late trochophore (14 days old) an organ of different origin and formation but of presumed photoreceptor type begins to develop among nerve cell bodies below the apex of the animal. This structure consists of an array of membranes developed from both cilia and microvilli. The cilia are of 9 + 2 configuration.     

Towards a ground pattern reconstruction of bivalve nervous systems: neurogenesis in the zebra mussel <Emphasis Type="Italic">Dreissena polymorpha</Emphasis>

Bivalvia is a taxon of aquatic mollusks that includes clams, oysters, mussels, and scallops. Within heterodont bivalves, Dreissena polymorpha is a small, mytiliform, freshwater mussel that develops indirectly via a planktotrophic veliger larva. Currently, only a few studies on bivalve neurogenesis are available, impeding the reconstruction of a ground pattern in Bivalvia. In order to inject novel data into this discussion, we describe herein the development of the serotonin-like and α-tubulin-like immunoreactive (lir) neuronal components of D. polymorpha from the early trochophore to the late veliger stage. Neurogenesis starts in the early trochophore stage at the apical pole with the appearance of one flask-shaped serotonin-lir cell. When larvae reach the veliger stage, four flask-shaped serotonin-lir cells are present in the apical organ. At the same time, the anlagen of the cerebral ganglia start to form at the base of the apical organ. From the apical organ, one pair of cerebro-visceral connectives projects posteriorly and connects to a posterior larval sensory organ that contains serotonin- and α-tubulin-like flask-shaped cells. Additional, paired serotonin-lir neurites originate from the apical organ and project into the velum. One unpaired stomatogastric serotonin-lir cell develops ventrally to the stomach at the veliger stage. The low number of serotonin-lir cells in the apical organ of bivalve veligers is shared with larvae of basally branching gastropods and scaphopods and is thus considered a feature of the last common ancestor of Conchifera, while the overall simplicity of the larval neural architecture appears to be a specific trait of Bivalvia.     

Neuromuscular development in Patellogastropoda (Mollusca: Gastropoda) and its importance for reconstructing ancestral gastropod bodyplan features

Within Gastropoda, limpets (Patellogastropoda) are considered the most basal branching taxon and its representatives are thus crucial for research into evolutionary questions. Here, we describe the development of the neuromuscular system in Lottia cf. kogamogai. In trochophore larvae, first serotonin‐like immunoreactivity (lir) appears in the apical organ and in the prototroch nerve ring. The arrangement and number of serotonin‐lir cells in the apical organ (three flask‐shaped, two round cells) are strikingly similar to those in putatively derived gastropods. First, FMRFamide‐lir appears in veliger larvae in the Anlagen of the future adult nervous system including the cerebral and pedal ganglia. As in other gastropods, the larvae of this limpet show one main and one accessory retractor as well as a pedal retractor and a prototroch muscle ring. Of these, only the pedal retractor persists until after metamorphosis and is part of the adult shell musculature. We found a hitherto undescribed, paired muscle that inserts at the base of the foot and runs towards the base of the tentacles. An apical organ with flask‐shaped cells, one main and one accessory retractor muscle is commonly found among gastropod larvae and thus might have been part of the last common ancestor.     

Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa

‘Trochophore’ is a term used in a strict sense for larvae having an opposed-band method of feeding, involving a prototroch and metatroch. Other ciliary bands such as a telotroch and neurotroch may be present. The trochophore has been proposed to represent the ancestral larval form for a group of metazoan phyla (including all members of the Spiralia). The name trochophore is also often applied to larvae that do not conform to the above definition. A cladistic analysis of spiralian taxa (with special reference to polychaete annelids), based on a suite of adult and larval characters, is used to assess several hypotheses: (1) that the trochophore (in a strict sense) is a plesiomorphic form for the Spiralia; (2) that die stricdy defined trochophore is plesiomorphic for members of the Spiralia such as the Polychaeta. The homology of each of the various separate ciliary bands of spiralian larvae, and features such as the apical tuft and protonephridia is also assessed. The results favour the conclusion that the trochophore, if defined as a feeding larval form using opposed bands, should not be regarded as an ancestral (= plesiomorphic) type for the Spiralia, or any other large taxon such as the Polychaeta or Mollusca. The evidence suggests that the various ciliary bands have differing evolutionary histories, and only the Echiura (possibly an annelid group) has members with the classical trochophore. The trochophore is re-defined as a larval form with a prototroch. This broad definition covers a wide variety of larvae, and matches the current usage more accurately than the restricted term. Features such as the neurotroch, telotroch and opposed-band feeding show convergence and reversals. The nature of the metatroch requires further investigation. The presence of a prototroch (and hence trochophore larvae) is used to identify an apomorphy-based taxon, Trochozoa, that includes the first ancestor to have evolved a prototroch and all its descendants. This minimally includes the Annelida [sensu lato), Echiura, Entoprocta, Mollusca and Sipuncula and is a less inclusive taxon than the Spiralia.     

Ultrastructure of the eyespot in three polychaete trochophore larvae (Annelida)

Summary The eyespot is structurally similar in trochophore larvae of Harmothoe imbricata, Serpula vermicularis and Spirobranchus giganteus. In the receptor cell parallel lamellae lie below a tuft of microvilli which extends into a hollow in one side of the pigment cell. In 1-eyed trochophores this space connects with the outside via a small pore. In eyes preserved during the day there is evidence of a membrane breakdown in both lamellae and microvilli as well as indications of a membrane-fragment disposal system involving the receptor cell, the pigment cell and the eyespot pore. The orientation of the eyespot of S. giganteus is the reverse of that found in S. vermicularis, a situation that may be associated with ecologically significant differences in behaviour.     

Larval development and post‐larval growth of Branchiomma bairdi (Annelida: Sabellidae) from a Mediterranean population

Branchiomma bairdi is a Caribbean fan worm introduced in several localities worldwide, including the Mediterranean Sea, where the species’ range has rapidly expanded. Reproduction in B. bairdi was previously investigated in both extra‐Mediterranean and Mediterranean areas, but no information is available on larval development and post‐larval growth. In the present article, we examined these features for a population from the Mar Grande of Taranto (Ionian Sea). The species is hermaphrodite, and fertilization occurs in situ. Mucus seems to play an important role in fertilization, and also in preserving eggs before fertilization. The trochophore stage develops within the mucus and after hatching, larvae swim for about 3 d before settlement. The trochophore showed a distinct prototroch and two red dorsolateral larval eyes. The pelagic stage takes only 96 h even though prototroch is maintained after settlement, disappearing at 5 d, when larvae showed three chaetigers and branchial crown consisted of four radioles. Some interesting observations concerning changes in the morphology of chaetae and in the number of uncini during growth are also reported, together with discussion of the development of stylodes, an important diagnostic feature in Branchiomma species identification.     

Ultrastructure of osmoregulatory organs in larvae of the brackish-water mosquito,Culiseta inornata (Williston)

The ultrastructure of the Malpighian tubules, ileum, rectum, anal canal, and anal papillae of larvae of the mosquito Culiseta inornata was examined. The Malpighian tubules, rectum, and anal papillae have many of the ultrastructural features characteristic of ion transport tissues, i.e., elaboration of the basal and apical membranes and a close association of these membranes with mitochondria. The Malpighian tubules possess two cell types, primary and stellate. The larval rectum of C. inornata is composed of a single segment containing a homogenous population of cells. In this respect, the larval rectum of C. inornata is distinct from that of saline-water species of Aedes. The cells in the larval rectum of C. inornata, however, closely resemble those of one cell type, the anterior rectal cells, of the saline-water mosquito Aedes campestris with regard to cell and nuclear size, the percentage of the cell occupied by apical folds, and mitochondrial density and distribution. No similarities can be found between the rectum of C. inornata and the posterior segment of the saline-water Aedes, which functions as a salt gland. On this basis, we have postulated that the rectum of C. inornata does not function as a site of hyperosmotic fluid secretion. The ultrastructure of the anal papillae of C. inornata is consistent with a role in ion transport. The significance of these findings to comparative aspects of osmoregulatory strategies in mosquito larvae is discussed.     

Identification of β integrin‐like‐ and fibronectin‐like proteins in the bivalve mollusk Mytilus trossulus

Integrins play a key role in the intermediation and coordination between cells and extracellular matrix components. In this study, we first determined the presence of the β integrin‐like protein and its presumptive ligand, fibronectin‐like protein, during development and in some adult tissues of the bivalve mollusc Mytilus trossulus. We found that β integrin‐like protein expression correlated with the development and differentiation of the digestive system in larvae. Besides the presence of β integrin‐like protein in the digestive epithelial larval cells, this protein was detected in the hemocytes and some adult tissues of M. trossulus. The fibronectin‐like protein was detected firstly at the blastula stage and later, the FN‐LP‐immunoreactive cells were scattered in the trochophore larvae. The fibronectin‐like protein was not expressed in the β integrin‐positive cells of either the veliger stage larvae or the adult mussel tissues and the primary hemocyte cell culture. Despite the β integrin‐ and fibronectin‐like proteins being expressed in different cell types of mussel larvae, we do not exclude the possibility of direct interaction between these two proteins during M. trossulus development or in adult tissues.     

The larval ocelli of Golfingia misakiana (Sipuncula, Golfingiidae) and of a pelagosphera of another unidentified species

 The inverse cerebral ocelli of the pelagosphera larva of Golfingia misakiana and of another unidentified larva are composed of two or three sensory cells and one supportive pigmented cell. The sensory cells bear an array of microvilli as well as a single cilium with poor undulation of its membrane; the photoreceptive organelles are regarded as the rhabdomeric type. A striking feature of these cells is the cores, which extend within the microvilli from the tip into the midregion of the cell. It is suggested that these structures are identical with the submicrovillar cisternae found in the cerebral inverse eyes of larvae of Polychaeta. The findings allow the conclusion that in the pelagosphera of the Sipuncula, contrary to the teleplanic veliger larvae of Gastropoda, a lengthy pelagic cycle is not correlated with the development of a ciliary photoreceptor. Additionally, it is assumed that the pigment cup ocelli in larvae of Sipuncula are homologous with the cerebral inverted pigment cup ocelli of larvae of Polychaeta. Accepted: 19 March 1997     

Anatomy of the larva of Amathia vidovici (Bryozoa: Ctenostomata) and phylogenetic significance of the vesiculariform larva

Amathia vidovici (Vesiculariidae) has a lecithotrophic coronate larva. The apical disc of A. vidovici larvae is more complex than that of other vesiculariids and includes a new cell type, which may be glial-like in function. A massive nerve nodule consists only of neural processes; as no ganglia or other evidence of interneurons were found, sensory cells apparently innervate their effectors directly. Putative synaptic junctions within the nerve nodule indicate that both receptor and effector cells send processes to this neuropile. Some 44 intercoronal cells of three types, two of which are new, are interspersed among the approximately 40 coronal cells. Juxtapapillary bodies, a unique sensory complex previously known only from Bowerbankia gracilis larvae, also occur in A. vidovici. A large refractile body, which is of uncertain function and is positioned near the center of the larva, is described for the first time. A comparison of vesiculariid larvae that have been studied at the ultrastructural level reveals that larvae of Amathia vidovici and Bowerbankia gracilis are more similar to each other than either is to B. imbricata. Differences between the two Bowerbankia species, however, may reflect relative detail of their study and differences in interpretation rather than intergenic plasticity. Nevertheless. a distinctive suite of larval characteristics are shared by other members of the family Vesiculariidae, justifying a specific name—vesiculariform—for their larvae. A number of the defining characteristics of vesiculariform larvae also appear in the carnosan superfamily Victorelloidae. This finding is consistent with arguments based on adult characteristics that the Victorelloidea are ancestral to the Vesicularioidea. If this geneology is correct, one can predict that those vesiculariform traits which originated in the victorellids are plesiomorphic not only to the Family Vesiculariidae but to all sister taxa placed in the Vesicularioidea. © 1993 Wiley-Liss, Inc.     

Ultrastructure of a cephalic sensory organ in larvae of the gastropod Phestilla sibogae (Aeolidacea, Nudibrachia)

The cephalic sensory organ is a superficial sensory receptor located between the velar lobes at the level of the shell aperture. Three cell types make up this sensory area: (1) six flask-shaped cells bearing numerous cilia; (2) adjacent supporting or accessory cells which have numerous, often branched, microvilli; and (3) vacuolated cells which occupy the center of the area. The flask-shaped cells appear to be the sensory units. These cells have a deep invaginated lumen, with cilia arising from the cell surface in the lumen oriented either toward the base of the lumen or toward the epidermal surface. These cilia, some of which extend slightly above the body surface, are presumed to be non-motile, as they lack (dynein?) arms on the axonemal A tubules and lack striated rootlets. The six flask cells are in intimate contact with the underlying cerebral ganglia and axons from each cell pass into ganglionic tissue. The supporting cells may be sensory, but no direct connection with the nervous system was seen. The function of the central vacuolated cells is not known. This cephalic organ may be a derivative of the original apical tuft of the trochophore stage.     

Larval Development and Metamorphosis in Sipuncula

In a brief review of development of the phylum Sipuncula, fourpatterns of development are recognized: (1) direct with no pelagicstage; (2) one larval stage, a lecithotrophic trochophore; (3)two larval stages, a lecithotrophic trochophore and a lecithotrophicpelagosphera; (4) two larval stages, a lecithotrophic trochophoreand a planktotrophic pelagosphera. Larval types and their metamorphosesare described, with special attention to the development andmorphology of the larval cuticle. In the majority of speciesstudied, the egg envelope is transformed into the larval cuticleat metamorphosis of the trochophore. The cuticle of many planktotrophicpelagosphera larvae is characterized by surface papillae ofdiverse form and pattern. The underlying cuticle in some speciesis composed of layers of fibers at right angles to one another.     

Stellate cells in the Malpighian tubules of Drosophila hydei and D. melanogaster larvae (Insecta, Diptera)

 The Malpighian tubules of Drosophila hydei and D. melanogaster larvae are composed of two types of cell, principal cells and stellate cells. In the anterior larval Malpighian tubules approximately 26% (D. hydei) and 18% (D. melanogaster), respectively, of all cells are stellate cells. In the larvae of D. melanogaster, the stellate cells are fenestrated and the hemolymph space and tubule lumen are separated only by the basal lamina. Injection of dyes into the hemolymph did not indicate any facilitated transfer of substances through the fenestrated cells. The principal cells of the distal segment are carbonic anhydrase positive indicating transport activity, whereas the stellate cells lack this enzyme. In the stellate cells of the transitional segment, the sodium content is strikingly high in comparison to the neighbouring principal cells and lumen where no sodium was detected. This finding indicates that stellate cells reabsorb sodium as supposed earlier in 1969 by Berridge and Oschman (Tissue Cell 1:247–272). Accepted: 12 February 1999     

Sensory endings of the ascidian static organ (Chordata,Ascidiacea)

Summary The ultrastructure of the static organ is examined in larvae of Diplosoma macdonaldi, a colonial ascidian, and Styela plicata, a solitary ascidian; the results are similar. As previous workers found, the cell body of a unicellular statocyte lies in the lumen of the sensory vesicle and contains the statolith. A narrow neck connects the cell body to an anchoring foot in the floor of the sensory vesicle. Two previously undescribed sensory endings project into the lumen just to the left of the statocyte, one anterior and one posterior to the neck. A network of fine processes from each ending contacts the statocyte body. It is proposed that movements of the statocyte cell body are detected by these endings. They arise from neurons in the ventral wall of the sensory vesicle that project axons to the visceral ganglion. The placement of the sensory endings may allow discrimination of the directon of statocyte deflection.Abbreviations ax axons - bb ciliary basal body - bl basal lamina - c cilium - cr striated ciliary rootlet - ec ependymal cells - en endoderm - h hemocoel - ly lysosome - mv microvilli - n neuron - nf neurofilaments - ns neck of the statocyte - sb statocyte cell body - sd sensory dendrite - sn sensory neuron - sp sensory processes - stf statocyte foot - svl sensory vesicle lumen - zo zonula occludens     

Neuronal development in larval mussel <Emphasis Type="Italic">Mytilus trossulus</Emphasis> (Mollusca: Bivalvia)

Although our understanding of neuronal development in Trochozoa has progressed substantially in recent years, relatively little attention has been paid to the bivalve molluscs in this regard. In the present study, the development of FMRFamide-, serotonin- and catecholamine-containing cells in the mussel, Mytilus trossulus, was examined using immunocytochemical and histofluorescent techniques. Neurogenesis starts during the trochophore stage at the apical extreme with the appearance of one FMRFamide-like immunoreactive (lir) and one serotonin-lir sensory cell. Later, five FMRFamide-lir and five serotonin-lir apical sensory cells appear, and their basal fibres form an apical neuropil. Fibres of two lateral FMRFamide-lir apical cells grow posteriorly and at the time that they reach the developing foot, the first FMRFamide-lir neurons of the pedal ganglia also appear. Subsequently, FMRFamide-lir fibres grow further posteriorly and reach the caudal region where neurons of the developing visceral ganglia then begin to appear. In contrast, the five apical serotonin-lir neurons do not appear to project outside the apical neuropil until the late veliger stage. Catecholamine-containing cells are first detected in the veliger stage where they appear above the oesophagus, and subsequently in the velum, foot, and posterior regions. Though neural development in M. trossulus partly resembles that of polyplacophorans in the appearance of the early FMRFamidergic elements, and of scaphopods in the appearance of the early serotonergic elements, the scenario of neural development in M. trossulus differs considerably from that of other Trochozoa (bivalves, gastropods, polyplacophorans, scaphopods and polychaetes) studied to date. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.