Larval morphology of the Nemertean Carcinonemertes epialti (Nemertea: Hoplonemertea)

The morphology of the newly hatched larva of Carcinonemertes epialti Coe has been examined by light and electron microscopy. The newly hatched larva is covered with cilia and measures about 110 μm in length. Four types of epidermal cells are recognizable: (1) Multiciliated cells, (2) vacuolated cells, (3) mucous cells, and (4) “knob cells”. The knob cells protrude from the posterior end of the larva and contain granules and bundles of microfilaments. The gut is incomplete and is located ventral to the bipartite proboscis. A bilobed brain and two subepidermal ocelli are found in the anterior end of the larva. The anterior and posterior cirri are composed of long, tightly appressed cilia that arise from an invagination of the epidermis at each end of the larva. The anterior cirrus is surrounded by two types of glandular cells. It is proposed that the knob cells have a role in larval attachment, combining the functions of the adhesive cells and anchor cells described in the duo-gland system of turbellarians. The cirri are believed to be larval sensory structures that function in substrate selection. Histological and ultrastructural observations suggest that the larvae of Carcinonemertes are relatively long lived and develop into juveniles without a drastic metamorphosis.     

Larval development in <Emphasis Type="Italic">Guancha arnesenae</Emphasis> (Porifera,Calcispongiae, Calcinea)

Larval development and follicle structure of a representative of the Calcinea (Calcispongiae) Guancha arnesenae from the White Sea have been studied for the first time at the ultrastructural level. The follicle in G. arnesenae has an unusual structure: it consists of trapezoid cells rich in phagosomes and a surrounding dense collagen layer. Follicular cells differentiate from choanocytes. Cleavage results in formation of a hollow, equal, non-polarized coeloblastula. Larval morphogenesis occurs by means of direct hollow blastula formation without any individual cell or cell layer movements. The coeloblastula (calciblastula) larva of G. arnesenae is completely ciliated. The larva also contains rare non-ciliated cells: vacuolar cells, bottle-shaped cells and free cells in a central cavity. The basal ciliary apparatus of larval cells includes the basal body, an accessory centriole oriented perpendicularly to it, the basal foot, and two cross-striated rootlets. A bundle of microtubules emerges from the side of the basal body, opposite to the basal foot, running parallel to the outer surface. All bundles of cells are parallel to each other and oriented towards the posterior larval pole, forming a transverse cytoskeletal system. Specialized intercellular junctions in the apical regions of all ciliated cells are revealed for the first time in a Calcispongiae larva. The central larval cavity contains symbiotic bacteria, which are included inside the embryo at the blastula stage.     

Lecithotrophic development and metamorphosis in the Indo-West Pacific brittle star Ophiomastix venosa (Echinodermata: Ophiuroidea)

Summary

The larval development of the ophiocomid ophiuroid Ophiomastix venosais described using SEM. The gastrula transforms into a uniformly ciliated early larva which progressively changes into a lecithotrophic late premetamorphic larva with a continuous bilateral ciliated band. This stage is short-lived and equivalent to a highly reduced ophiopluteus. Comparisons between O. venosa and other ophiuroid species whose development has been investigated suggest that, whatever the developmental mode (lecithotrophic or planktotrophic), a pluteus stage always occurs in ophiuroids with planktonic development. Two metamorphic stages were identified, the late metamorphic larva differing from the early one by the closure of the larval mouth. The appearance of the permanent mouth marks the end of the metamorphosis. The postlarva still possesses remnants of larval features. The transformation of the reduced ophiopluteus into a barrel-shaped metamorphic larva with transverse ciliated bands, a vitellaria larva, is followed. The possible occurrence of a unique type of metamorphic larva in non-brooding ophiuroids is discussed. Verification of this, however, needs further SEM investigations on metamorphic larva from species having “regular” planktotrophic development.     

Attachment and metamorphosis of the cheilo-ctenostome bryozoan bugula neritina (linné)

The structure, attachment and subsequent metamorphosis of larvae of the marine bryozoan Bugula neritina were studied by light and electron microscopy. Two points of larval anatomy are of special significance to proper interpretation of the metamorphosis:

• 1 Two cytologically similar blastemal tissues, each laden with free ribosomes, occur as parts of the apical organ complex. The upper blastema directly contacts the larval surface, forming the non-ciliated rows of the apical organ. The lower blastema is internal and is oral to and contiguous with the upper blastema.
• 2 The epidermal tissues of the larva are joined in the following sequence, beginning at the aboral pole: a. apical organ complex; b. apical-connecting cell; c. infolded pallial sinus epithelium; d. vesicular-connecting cell; e. aboral vesicular epithelium; f. corona; g. oral vesicular epithelium; and i., j., and k. internal sac neck, wall and roof regions.

The initial stages of metamorphosis involve a complex sequence of morphogenetic movements, including:

• 1 eversion of the internal sac, permanently attaching the larva to the substrate;
• 2 inrolling of the aboral vesicular epithelium, corona, oral vesicular and ciliated epithelia, and neck region of the internal sac into the larval interior; concomitantly the pallial sinus epithelium evaginates;
• 3 loss of connection between the invaginated tissues and the surface;
• 4 fusion of the pallial sinus epithelium with the wall region of the internal sac, maintaining the integrity of the body surface;
• 5 retraction of the apical organ complex and invagination of the pallial sinus epithelium with the simultaneous elevation of the internal sac wall region to the aboral pole.

At the conclusion of these events the preancestrular surface is covered by the wall and roof regions of the internal sac. Cells of the wall region form the epidermis of the body wall except for the attachment disc and secrete a cuticular exoskeleton that is secondarily calcified; the attachment disc is formed by the roof region of the internal sac. Internally, the ectodermal upper blastema differentiates into the lophophore and digestive tract of the ancestrular polypide, while the lower blastema forms the lining of the lophophoral coelom and the splanchnic (but not the somatic) lining of the visceral coelom. The visceral somatic peritoneum is formed from cells that may originate from the mesodermally derived pigmented cells of the larva to which they are similar in pigmentation and cytology. Such a composite derivation of a coelomic lining has not been described previously.     

Three‐dimensional fate mapping of larval tissues through metamorphosis in the glass sponge Oopsacas minuta

The tissue of glass sponges (Class Hexactinellida) is unique among metazoans in being largely syncytial, a state that arises during early embryogenesis when blastomeres fuse. In addition, hexactinellids are one of only two poriferan groups that already have clearly formed flagellated chambers as larvae. The fate of the larval chambers and of other tissues during metamorphosis is unknown. One species of hexactinellid, Oopsacas minuta, is found in submarine caves in the Mediterranean and is reproductive year round, which facilitates developmental studies; however, describing metamorphosis has been a challenge because the syncytial nature of the tissue makes it difficult to trace the fates using conventional cell tracking markers. We used three‐dimensional models to map the fate of larval tissues of O. minuta through metamorphosis and provide the first detailed account of larval tissue reorganization at metamorphosis of a glass sponge larva. Larvae settle on their anterior swimming pole or on one side. The multiciliated cells that formed a belt around the larva are discarded during the first stage of metamorphosis. We found that larval flagellated chambers are retained throughout metamorphosis and become the kernels of the first pumping chambers of the juvenile sponge. As larvae of O. minuta settle, larval chambers are enlarged by syncytial tissues containing yolk inclusions. Lipid inclusions at the basal attachment site gradually became smaller during the six weeks of our study. In O. minuta, the flagellated chambers that differentiate in the larva become the post‐metamorphic flagellated chambers, which corroborate the view that internalization of these chambers during embryogenesis is a process that resembles gastrulation processes in other animals.     

Testing attachment point theory: diatom attachment on microtextured polyimide biomimics

Abstract

This paper explores diatom attachment to a range of laser etched polyimide surfaces to directly test ‘attachment point theory’. Static bioassays were conducted on microtextured polyimide surfaces using four diatom species, Fallacia carpentariae, Nitzschia cf. paleacea, Amphora sp. and Navicula jeffreyi with cell sizes ranging from 1 – 14 μm. The microtextured polyimides were modelled from natural fouling resistant bivalve surfaces and had wavelengths above, below and at the same scale as the diatom cell sizes. Diatoms attached in significantly higher numbers to treatments where the numbers of attachment points was highest. The lowest diatom attachment occurred where cells were slightly larger than the microtexture wavelength, resulting in only two theoretical points of attachment. The results support attachment point theory and highlight the need to address larval/cell size in relation to the number of attachment points on a surface. Further studies examining a range of microtexture scales are needed to apply attachment point theory to a suite of fouling organisms and to develop structured surfaces to control the attachment and development of fouling communities.     

How whale and dolphin barnacles attach to their hosts and the paradox of remarkably versatile attachment structures in cypris larvae

How larvae of whale and dolphin epibionts settle on their fast-swimming and migrating hosts is a puzzling question in zoology. We successfully reared the larvae of the whale and dolphin barnacle Xenobalanus globicipitis to the cyprid stage. We studied the larval developmental ecology and antennular morphology in an attempt to assess whether an epibiotic lifestyle on this extreme substratum entails any unique larval specializations. Morphological parameters were compared with five other barnacle species that also inhabit extreme substrata. We found no larval specializations to a lifestyle associated with marine mammals. The external morphology of the antennules in Xenobalanus cyprids is morphologically similar to species from strikingly different substrata. We found variation only in the structures that are in physical contact with the substratum, i.e., the third segments carrying the villi-covered attachment disc. The third segments of the Xenobalanus cyprid antennules are not spear-shaped as in the stony coral barnacles, which are here used to penetrate the live tissue of their hosts. The presence of a cyprid cement gland implies that Xenobalanus uses cement protein when attaching to its cetacean host. Naupliar instars developed outside of the mantle cavity, indicating dispersal is planktonic. Our results militate against the idea that the cyprids settle during ocean migrations of their hosts. We suggest cyprids settle during coastal aggregations of the cetacean hosts. We conclude that the ecological success of barnacles has ultimately depended on a larva that with little structural alteration possesses the ability to settle on an amazingly wide array of substrata, including cetaceans.

     

Phytohormones in Japanese Mugwort Gall Induction by a Gall-Inducing Gall Midge

A variety of insect species induce galls on host plants. Liquid chromatographic/tandem mass spectrometric analyses showed that a gall midge (Rhopalomyia yomogicola) that induces galls on Artemisia princeps contained high levels of indole-3-acetic acid and cytokinins. The gall midge larvae also synthesized indole-3-acetic acid from tryptophan. Close observation of gall tissue sections indicated that the larval chamber was surrounded by layers of cells having secondary cell walls with extensive lignin deposition, except for the part of the gall that constituted the feeding nutritive tissue which was composed of small cells negatively stained for lignin. The differences between these two types of tissue were confirmed by an expression analysis of the genes involved in the synthesis of the secondary cell wall. Phytohormones may have functioned in maintaining the feeding part of the gall as fresh nutritive tissue. Together with the results in our previous study, those presented here suggest the importance of phytohormones in gall induction.     

Morphogenesis accompanying larval metamorphosis in Plakina trilopha (Porifera, Homoscleromorpha)

Morphological investigations of morphogenesis accompanying the metamorphosis of the cinctoblastula larva of poriferan Plakina trilopha (Homoscleromorpha) have been made. The larva possesses a distinct columnar epithelium which subdivides into three cellular areas: antero-lateral, postero-lateral, and posterior one. Characteristic morphological features of the cells in each area can be used as natural markers when tracing the fate of larval cells during metamorphosis. The ciliated epithelium of the larva is transformed directly into choanoderm and pinacoderm, without losing its organization. This transformation is a peculiar feature of the metamorphosis in Homoscleromorpha. Metamorphosis in P. trilopha is based on epithelial morphogenesis and includes the mechanisms of flattening of the exopinacoderm, evagination and invagination of larval epithelium in the course of the development of the rhagon aquiferous system. The flattening of larval cells during exopinacoderm formation in metamorphosing P. trilopha is a common change of cell shape during epithelial morphogenesis of this species. The separation of proximal fragments of cells has been observed here. This phenomenon, that we have called “cytoplasmic shedding”, appears to play an important role in the change of epithelial cell shape in P. trilopha. Mechanism of epithelial–mesenchymal transition, i.e., ingression of epithelial ciliated cells into the cavity of the metamorphosing larva of P. trilopha participates in mesohylar cell origin.     

Fine structure of the doliolaria larva of the feather star Florometra serratissima (Echinodermata: Crinoidea), with special emphasis on the nervous system

The epidermis of the doliolaria larva of the Florometra serratissima is differentiated into distinct structures including an apical organ, adhesive pit, ganglion, ciliary bands, nerve plexus, and vestibular invagination. All these structures possess unique cell-types, suggesting that they are functionally specialized in the larva, except the vestibular invagination that becomes the postmetamorphic stomodeum. The epidermis also contains yellow cells, amoeboid-like cells, and secretory cells. The enteric sac, hydrocoel, axocoel, and somatocoels have differentiated but are probably not functional in the doliolaria stage. Mesenchymal cells, around the enteric sac and coeloms, appear to be actively secreting the endoskeleton and connective tissue fibers. The nervous system is composed of a nerve plexus, ganglion, and sensory receptor cells in the apical organ. The apical organ is a larval specialization of the anterior end; the ganglion is located in the base of the epidermis at the anterior dorsal end of the larva. The nerve plexus underlies most of the epidermis, although it is more prominent in the anterior region. Here, processes from sensory receptor cells of the apical organ, as well as those from nerve cells, contribute to the plexus. These processes contain one or a combination of organelles including vesicles, vacuoles, microtubules, and mitochondria. The configuration of glyoxylic acid-induced fluorescence, revealing catecholamine activity, correlates to the apical organ, nerve cells, and nerve plexus. Morphological evidence suggests that the nervous system may function in initiation and control of settlement, attachment, and metamorphosis. The crinoid larval nervous system is discussed and compared to that found in other larval echinoderms.     

Ultrastructure of mesoderm formation and development in Membranipora membranacea (Bryozoa: Gymnolaemata)

Mesoderm origin in Bryozoa is largely unknown. In this study, embryonic and early larval stages of Membranipora membranacea, a bryozoan exhibiting a planktotrophic cyphonautes larva, are investigated using mainly ultrastructural techniques. Shortly after the onset of gastrulation, an ectodermal cell, which is situated centrally at the prospective anterior pole of the larva, can be recognized by its constricted apical surface and enlarged basal part. It is also distinct from other ectodermal cells by the composition of its cytoplasm. In later stages, it has left the epidermis, lost its epithelial character, and is situated subepithelially, between the basal sides of the ectodermal and endodermal sheets. A blastocoelic cavity is not present at this stage. This cell divides and gives rise to a group of cells forming a muscular and neuronal strand at the anterior side of the larva. The majority of the larval musculature originates from this ingression. Despite this evidence for an ectodermal origin, additional sources of mesoderm can so far not be excluded. The literature on mesoderm origin in Bryozoa is reviewed and the results are compared to known data from other metazoan taxa.     

Growth and development of larvae and galls of Urophora cardui (Diptera,Tephritidae) on Cirsium arvense (Compositae)

Summary The tephritid fly Urophora cardui induces a large multi-chambered gall within the stems of Cirsium arvense. Three distinct phases of gall development have been identified as initiation, growth, and maturation. During initiation the insect gains control of tissue development and during the gall's growth phase parenchyma cells proliferate rapidly surrounding the larvae with thick layers of cells. Patches of primary nutritive cells appear along the surface of larval chambers during the growth phase but few of these cells are consumed. In the gall's maturation phase, thick layers of secondary nutritive cells appear around the surface of larval chambers and the remaining gall parenchyma lignifies. Secondary nutritive cells are the primary food of U. cardui.The gall expands rapidly during the growth phase then abruptly slows at the beginning of the maturation phase. Rate of gall growth is dependent upon the number of larvae per gall but the number of larvae does not affect duration of this phase.Larvae remain in the second instar throughout the growth phase and grow slowly. Once the gall enters the maturation phase and the secondary nutritive cells appear, the larvae moult to the third instar and grow quickly. Larvace attain over 98% of their final weight during the maturation phase and consume all secondary nutritive cells.It is postulated that larvae do not feed extensively on primary nutritive cells since these cells play a key role in gall morphogenesis. The appearance of secondary nutritive cells stimulates larval feeding at a time when gall growth and development is finished.     

Xenochironomus canterburyensis (Diptera: Chironomidae), a commensal of Hyridella menziesi (Lamellibranchia) in Lake Taupo; features of pre-adult life history

Abstract

The larvae and pupae of the univoltine chironomid Xenochironomus canterburyensis (Freeman) are inquiline commensals of the freshwater mussel Hyridella menziesi (Gray). The 1st- and 2nd-instar larvae enter the mantle/valve cavity of the mussel in midsummer, and by early winter migrate as 3rd-instar larvae to the posterior end of the valve to lodge near its margin beside the inhalant siphon. During the spring, growth of the periostracum of the valve margin between the larva and the mantle of the mussel leaves the 4th-instar larva outside the mantle/valve cavity, where it pupates before leaving the mussel for the lake surface and adult emergence.     

Changes in the timing of mantle formation and larval life history traits in linguliform and craniiform brachiopods

The distribution of embryonic and larval mantles is documented in linguliform and craniiform brachiopods. Criteria are presented for identifying these mantle types. The mantle type is related to planktotrophic and lecithotrophic larval life history patterns. In the Linguliformea and Craniiformea, all Lower Palaeozoic families with adequate preservation had larval mantles, indicating the presence of a planktotrophic larva. Heterochronic changes in the time of mantle origin, from the larval to the embryonic stage of development, has occurred several times. In the Lingulidae this change appears to have taken place at about the time the family originated in the Devonian and has been retained in extant genera. The family Discinidae has also retained a planktotrophic larval stage from the Lower Palaeozic to the present. The extant genus Crania in the Craniidae has a short-lived lecithotrophic larva that lacks a mantle. Through the Lower Jurassic, this family had planktotrophic larvae with a larval shell. During the Upper Jurassic, genera with a lecithotrophic larva that lacked a larval shell began to appear; however, the last genera in this family with a planktotrophic larva and a larval shell did not become extinct until the Tertiary.     

Oogenesis and larval development of Ephydatia fluviatilis (Porifera,Spongillidae)

Summary In Ephydatia fluviatilis young oocytes already appear in autumn. They pass the winter in the highly reduced sponge, but vitellogenesis and further development do not take place before following spring. The fact that the young oocytes appear before the normal period of reproduction makes E. fluviatilis different from all other local freshwater sponges, which reduce totally in autumn. E. fluviatilis seems to be a gonochorist. The oocytes originate from archaeocytes and during the first growth phase they reach a diameter of approximately 40 m. In the second growth phase the oocyte is enclosed in a single-layered follicle epithelium and grows to 170–180 m by phagocytosis of trophocytes. The fully developed egg cell finally shows a distinct layering of the incorporated yolk material. Cleavage is totally equal to unequal so that macro- and micromeres appear in some cleavage stages. Cleavage leads to a solid embryo consisting of uniform cells. At this stage of development the first scleroblasts appear. As the cells develop they are surrounded by companion cells, managing the transport of the scleroblasts. The further development to the larva is marked by the appearance of the larval cavity, typical for larvae of Spongillids, which finally occupies about half the volume of the larva at emergence. The periphery of the larva consists of a single-layered ciliated epithelium. After emergence the larva forms flagellated chambers, which are integrated into the primordia of the excurrent canal system. This system connects with the larval cavity and ensures that it becomes part of the excurrent canal system of the young sponge. Particularly in the region of the larval cavity the ciliated epithelium of the free larva is reduced. Here a new larval surface epithelium is formed by pinacocytes.     

Larval Behavior and Post-Larval Development in Parasmittina nitida Morphotype B (Bryozoa: Cheilostomata)

Larval behavior and metamorphosis in Parasmittina nitida morphotypeB from the Gulf of Mexico has been studied. The larvae havetwo basic types of movement: (1) a clockwise-counterclockwisemovement about the aboral-oral axis of the lobular larval formresulting in either slow horizontal or rapid vertical movement,and (2) a directed horizontal movement of the creeping larvalform, whereby either the oral lobe is pressed against the substrateor the aboral-oral axis is tilted forward. In both forms, thevibratile plume of the pyriform organ complex extends the leadingedge of the larva. Metamorphosis was observed with Nomarskidifferential interference microscopy in living specimens andwith scanning electron microscopy in fixed specimens. Polypidedevelopment— in particular, the formation and diminutionof the nutritive mass, the differentiation of the polypide rudiment,diaphragm, vestibular glands, operculum, major components ofthe musculature and alimentary canal, and the early stages ofastogenetic growth—is described. The tata ancestrula ofthis species is characterized by a frontal wall calcified distallyto the aperture, which is surrounded by nine erect spines. Thepolypide feeds actively within seven to eight days after theonset of larval attachment and metamorphosis under laboratoryconditions of 22°C.     

Development of the musculature in the limpet Patella (Mollusca, Patellogastropoda)

 Whole-mount technique using fluorescent-labelled phalloidin for actin staining and confocal laser scanning microscopy as well as semi-thin serial sectioning, scanning and transmission electron microscopy were applied to investigate the ontogeny of the various muscular systems during larval development in the limpets Patella vulgata L. and P. caerulea L. In contrast to earlier studies, which described a single or two larval shell muscles, the pretorsional trochophore-like larva shows no less than four different muscle systems, namely the asymmetrical main head/foot larval retractor muscle, an accessory larval retractor with distinct insertion area, a circular prototroch/velar system, and a plexus-like pedal muscle system. In both Patella species only posttorsional larvae are able to retract into the shell and to close the aperture by means of the operculum. Shortly after torsion the two adult shell muscles originate independently in lateral positions, starting with two fine muscle fibres which insert at the operculum and laterally at the shell. During late larval development the main larval retractor and the accessory larval retractor become reduced and the velar muscle system is shed. In contrast, the paired adult shell muscles and the pedal muscle plexus increase in volume, and a new mantle musculature, the tentacular muscle system, and the buccal musculature arise. Because the adult shell muscles are entirely independent from the various larval muscular systems, several current hypotheses on the ontogeny and phylogeny of the early gastropod muscle system have to be reconsidered. Received: 23 June 1998 / Accepted: 25 November 1998     

Optimal clutch size of the chestnut gall-wasp,Dryocosmus kuriphilus yasumatsu (Hymenoptera: Cynipidae)

Optimal clutch size of the chestnut gall-wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), was examined in galls on wild and resistant chestnut trees in 1988 and 1989. The rate of escape success of newly-emerged adults from galls was an average of 60%, irrespective of cell numbers per gall. Dry mass per cell of a gall (as an index of nutritive condition) decreased with increasing cell number per gall, but was proportional to the mean number of mature eggs of new adults per gall. The number of cells per gall that occurred most frequently did not agree with that attained by the maximum survival rate from young larva to adult emergence of the gall-wasp. This discrepancy was examined from the viewpoint of three factors: 1) quality of offspring, 2) defensive response of the host plant causing mortality of the gall-wasp before cell formation, and 3) fitness per gall vs. fitness per egg. It is concluded that the third factor is most likely to be the one best in explaining the discrepancy.