Fine Structure and Function of Pharynx Cilia in Glossobalanus minutus Kowalewsky (Enteropneusta)

Two kinds of cilia have been observed in the pharynx of Glossobalanus minutus Kowalewsky. From the present study, a ciliary specialization can be found in order to move a determinate substance, i.e. mucus or water. Mucus-moving cilia (type I cilia) have a single basal centriole and poorly developed ciliary rootlets. Their tips are rounded, bearing an inner, asymmetrical cap attached to some tubules. Water-moving cilia (type II cilia) are exclusively located at lateral epithelia of branchial bars, giving rise to the water current through the gills. They have two basal centrioles, proximal and distal, and a complex system of ciliary rootlets made up of a principal rootlet, a secondary or accessory rootlet and a 'fan' rootlet. The tips of type II cilia have a long process with some tubules inside. All basal structures are precisely orientated in order to assure a good coordination of ciliary beat. The possible functional significance of ciliary substructure is also discussed. From these observations a model for mucus and water currents through gill slits is postulated.     

Blood Vessels and Related Structures in the Gill Bars of Glossobalanus minutus (Enteropneusta)

The branchial circulatory system of Glossobalanus minutus (Enteropneusta) is investigated by means of transmission electron microscopy. Primary gill bars, or septa, have a single blood vessel longitudinally located along the outer edge of the bar. Secondary gill bars, or tongue bars, show a vessel in their inner, pharyngeal edge. The walls of both vessels are made up of the basement membranes of surrounding epithelia, lacking an endothelium. No definite limits between the vessel lumen and the skeletal rods inside the bars can be seen. Furthermore, the blood seems to penetrate into the rods of both primary and secondary gill bars. In the secondary bars such a phenomenon gives rise to the so-called 'lateral vessels' reported in the light microscopical literature. The significance of these observations is discussed, with special reference to the gill circulatory system of amphioxus, which seems to be strongly similar from a morphological and ultrastructural point of view.     

Electron microscopic study of the intestinal epithelium of Saccoglossus mereschkowskii (Enteropneusta, Hemichordata)

Epithelium of the hepatic region of the intestine in Saccoglossus mereschkowskii, a representative of enteropneusts (Enteropneusta, Hemichordata) standing at the base of Chordata, has been investigated using electron microscope. The ultrastructure of ciliated and granular epithelial cells, elements of the intraepithelial nerve layer, and intercellular junctions have been characterized. The data concerning details of the organization of the ciliary apparatus and rootlets system are presented. It is justified the presence of complicated supporting construction of cilia which performs a mechanical stabilizing function and possibly also provide synchronization of ciliary movements. The presence of cilia with two centrioles is considered as an adaptation to high functional load on ciliary apparatus. Well developed bundles of myofilaments are found in the cytoplasm of the basal portions of ciliary cells that characterizes these cells as myoepithelial. The features indicating the role of ciliary cells in absorption are described. The capability of these cells to balloon-like secretion is considered. Data on the accumulation of food reserves in the form of lipid droplets and glycogen in the cell cytoplasm are presented. Ciliated cells are characterized by their function as ciliated secretory-absorptive myoepithelial cells. Based on the location of secretory granules both in the apical and basal portions of granular cells, an exocrine-endocrine function of these cells has been suggested. Typical endocrine cells in the intestinal epithelium of S. mereschkowskii are absent. Several types of granules in the nerve fibers cytoplasm are described. Junctions between the nerve fibers and basal portions of ciliary and granular epithelial cells are found. Nerve regulation of contractile and secretory functions of epithelial cells is supposed. The presence of the regulatory nerve-endocrine system that includes receptor cells of open type, secretory endocrine-like cells and nerve elements of nerve layer is supposed in the intestinal epithelium of enteropneusts.     

Diversification of acorn worms (Hemichordata, Enteropneusta) revealed in the deep sea

Enteropneusts (phylum Hemichordata), although studied extensively because of their close relationship to chordates, have long been considered shallow-water, burrowing animals. The present paper more than doubles the number of enteropneust species recorded in the deep sea based on high-resolution imaging and sampling with remotely operated vehicles. We provide direct evidence that some enteropneusts are highly mobile-using changes in posture and currents to drift between feeding sites-and are prominent members of deep, epibenthic communities. In addition, we provide ecological information for each species. We also show that despite their great morphological diversity, most deep-living enteropneusts form a single clade (the rediagnosed family Torquaratoridae) on the basis of rDNA sequences and morphology of the proboscis skeleton and stomochord. The phylogenetic position of the torquaratorids indicates that the group, after evolving from near-shore ancestors, radiated extensively in the deep sea.     

Feeding Characteristics of Deep-Sea Acorn Worm (Hemichordata,Enteropneusta, Torquaratoridae) from the Bering Sea

Doklady Biological Sciences - Deep-sea hemichordates Torquaratoridae gen. sp. reach high abundance up to 12 spec. m–2 at the depths of 1830–2130 m on the slope of the Volcanologists...     

On the Fine Structure of the Alimentary Tract of Cephalodiscus gracilis (Pterobranchia,Hemichordata)

The U-shaped alimentary tract of Cephalodiscus is of exclusively epithelial structure; on the basis of fine structural criteria the entire tract can be divided into two large subdivisions: an anterior one with mouth, mouth cavity, pharynx and oesophagus, and a posterior one with stomach and intestine. The anterior subdivision is built up of a relatively uniform, innervated, pseudostratified, ciliated epithelium with mucus cells which are concentrated in the initial parts of the mouth cavity. Cilia and mucus presumably constitute a mechanism transporting food particles into the stomach. In the area of the gill slits specific vacuolated cells occur which may lend rigidity to the walls of the slits. The gastric epithelium consists of prismatic cells characterized by, among others, large inclusion bodies, which may represent digestive vacuoles, small dense rod-shaped granules and an elaborate system of microridges, at the base of which abundant endocytotic vesicles occur. The dorsal gastric pouch contains cells rich in rough ER and secretory granules, probably containing digestive enzymes. Thus morphological evidence points both to intra- and extracellular digestion. The intestinal epithelium resembles that of the stomach, however, it is lower, its organelles are fewer and it bears, beside cilia, mainly microridges, which towards its distal end become sparse. Both in the gastric and intestinal epithelium small granulated cells have been found, which presumably represent endocrine cells.     

The First Discovery of Trematodes (Digenea) in the Deep-Sea Acorn Worms Torquaratoridae (Hemichordata,Enteropneusta)

Doklady Biological Sciences - Trematodes found in the enteropneust hemichordates are described for the first time. Metacercariae have been found in the trunk coelom, in the collar coelom, in the...     

Structure,Ultrastructure, and Function of the Preoral Heart-Kidney in Saccoglossus kowalevskii (Hemichordata,Enteropneusta) Including New Data on the Stomochord

The heart-kidney of Saccoglossus kowalevskii, which is situated within the anterior preoral proboscis coelom (protocoel), consists of the stomochord, pericardium, heart sinus, and glomerulus. The stomochord, a diverticulum of the gut, is characterized by vacuolated epithelial cells surrounded by basal lamina and connective tissue. The pericardium, a myoepithelium, lies dorsal to the central heart sinus. Opening into the protocoel and connecting with the outside via the proboscis pore is the protocoel duct, which is, in part, composed of multiciliated absorptive epithelial cells. Perfusion of the dorsal trunk vessel with vital dyes reveals a rapid flow of blood into the glomerular blood vessels. Examination of the permeability characteristics of the extracellular matrix underlying the glomerular podocytes reveals the movement of iron dextran (mol. wt 5000 daltons) from the central heart sinus into the protocoel. Iron dextran uptake by glomerular cells and protocoel lining cells is demonstrated. These results suggest that vascular fluid is filtered by the glomerulus, producing a primary urine in the protocoel which may be modified as it passes over the peritoneum, through the protocoel duct, and out of the proboscis pore. New data concerning the morphology of the stomochord are presented. The controversial homology between the hemichordate stomochord and the chordate notochord is addressed.     

Molecular Phylogeny and Ultrastructure of Caliculium glossobalani n. gen. et sp. (Apicomplexa) from a Pacific Glossobalanus minutus (Hemichordata) Confounds the Relationships Between Marine and Terrestrial Gregarines

Gregarines are a diverse group of apicomplexan parasites with a conspicuous extracellular feeding stage, called a “trophozoite”, that infects the intestines and other body cavities of invertebrate hosts. Although the morphology of trophozoites is very diverse in gregarines as a whole, high degrees of intraspecific variation combined with relatively low degrees of interspecific variation make the delimitation of different species based on trophozoite morphology observed with light microscopy difficult. The coupling of molecular phylogenetic data with comparative morphology has shed considerable light onto the boundaries and interrelationships of different gregarine species. In this study, we isolated a novel marine gregarine from the hepatic region of a Pacific representative of the hemichordate Glossobalanus minutus, and report the first ultrastructural and molecular data from any gregarine infecting this distinctive group of hosts. Molecular phylogenetic analyses of an SSU rDNA sequence derived from two single‐cell isolates of this marine gregarine demonstrated a strong and unexpected affiliation with a clade of terrestrial gregarines (e.g. Gregarina). This molecular phylogenetic data combined with a comparison of the morphological features in previous reports of gregarines collected from Atlantic representatives of G. minutus justified the establishment of a new binomial for the new isolate, namely Caliculium glossobalani n. gen. et sp. The molecular phylogenetic analyses demonstrated a clade of terrestrial gregarines associated with a sequence acquired from a marine species, which suggest that different groups of terrestrial/freshwater gregarines evolved independently from marine ancestors.     

Fine Structure of Tentacles,Arms and Associated Coelomic Structures of Cephalodiscus gracilis (Pterobranchia,Hemichordata)

The tentacles of the pterobranch Cephalodiscus, a hemisessile ciliary feeder, originate from the lateral aspects of the arms and are covered by an innervated epithelium, the majority of its cells bearing microvilli. Each side of a tentacle has two rows of ciliated cells and additional glandular cells. The coelomic spaces in the tentacles are lined by cross-striated myoepithelial cells, allowing rapid movements of the tentacles. One, possibly two, blood vessels accompany the coelomic canal. On their outer sides the arms are covered by a simple ciliated epithelium with intra-epithelial nerve fibres; the inner side is covered by vacuolar cells. On both sides different types of exocrine cells occur. The collar canals of the mesocoel are of complicated structure. Ventrally their epithelium is pseudostratified and ciliated; dorsally it is lower and forms a fold with specialized cross-striated myoepithelial cells of the coelomic lining. Arms, tentacles, associated coelomic spaces and the collar canal of the mesocoel are considered to be functionally interrelated. It is assumed that rapid regulation of the pore width is possible and even necessary when the tentacular apparatus is retracted, which presumably leads to an increase of hydrostatic pressure in the coelom.     

An Anatomical Description of a Miniaturized Acorn Worm (Hemichordata,Enteropneusta) with Asexual Reproduction by Paratomy

The interstitial environment of marine sandy bottoms is a nutrient-rich, sheltered habitat whilst at the same time also often a turbulent, space-limited, and ecologically challenging environment dominated by meiofauna. The interstitial fauna is one of the most diverse on earth and accommodates miniaturized representatives from many macrofaunal groups as well as several exclusively meiofaunal phyla. The colonization process of this environment, with the restrictions imposed by limited space and low Reynolds numbers, has selected for great morphological and behavioral changes as well as new life history strategies.Here we describe a new enteropneust species inhabiting the interstices among sand grains in shallow tropical waters of the West Atlantic. With a maximum body length of 0.6 mm, it is the first microscopic adult enteropneust known, a group otherwise ranging from 2 cm to 250 cm in adult size. Asexual reproduction by paratomy has been observed in this new species, a reproductive mode not previously reported among enteropneusts.Morphologically, Meioglossus psammophilus gen. et sp. nov. shows closest resemblance to an early juvenile stage of the acorn worm family Harrimaniidae, a result congruent with its phylogenetic placement based on molecular data. Its position, clearly nested within the larger macrofaunal hemichordates, suggests that this represents an extreme case of miniaturization. The evolutionary pathway to this simple or juvenile appearance, as chiefly demonstrated by its small size, dense ciliation, and single pair of gill pores, may be explained by progenesis. The finding of M. psammophilus gen. et sp. nov. underscores the notion that meiofauna may constitute a rich source of undiscovered metazoan diversity, possibly disguised as juveniles of other species.     

Morphology and development of a new species of Balanoglossus (Hemichordata: Enteropneusta: Ptychoderidae) from Shimoda, Japan

The morphology and development of a new species of the genus Balanoglossus belonging to the family Ptychoderidae are described in detail. This acorn worm was collected from the sandy seashore in the cove near Shimoda Marine Research Center, University of Tsukuba (Shimoda, Shizuoka Prefecture, Japan). This acorn worm is easily distinguished from other balanoglossids by a characteristic hepatic region. There are two kinds of hepatic saccules: large, dark-colored saccules in the anterior region and small, light-colored saccules in the posterior region. Between the two subregions of the hepatic region, there is a small region that has no or tiny saccules. This species does not form distinct burrows or mounds of casts. The breeding season is in winter. The process of embryogenesis from fertilization to metamorphosis was observed. A shift in seawater temperature from about 13 degrees C to about 9 degrees C induced gamete release. Two days after fertilization, embryos hatched and became typical feeding tornaria larvae. Two months after fertilization these larvae metamorphosed into juveniles and began their benthic life.     

Fine Structure of Heart,Pericardium and Glomerular Vessel in Cephalodiscus gracilis M'Intosh, 1882 (Pterobranchia,Hemichordata)

Heart, pericardium and glomerular vessel of Cephalodiscus gracilis have been studied with the electron microscope. The lumen of the heart is lined by a basal lamina and an associated epithelium, composed of myoepithelial cells with well developed thin and thick myofilaments. The heart is located in the pericardial cavity, which is deliminated by the pericardium. The latter is composed of two flat layers of myoepithelia with fused basal laminae. The outer layer of the pericardium is the protocoelomic lining, and the inner layer is the ‘parietal’ pericardial epithelium. The myoepithelium forming the heart wall can be considered to represent the ‘visceral’ pericardial epithelium. The spacious glomerular vessel is lined by a basal lamina, on which typical podocytes rest. These cells indicate that ultrafiltration takes place through the wall of the glomerular vessel. The lumen of the vessel contains fine granular material (presumably precipitated blood proteins), fibrils with a faint cross striation, suggesting that they represent collagen, and stellate cells, which in part line the vessel. Since ultrafiltration requires hydrostatic pressure, it is inferred that the blood flow is from the dorsal region then through the heart and into the glomerular vessel.     

Saccoglossus testa from the Mazon Creek fauna (Pennsylvanian of Illinois) and the evolution of acorn worms (Enteropneusta: Hemichordata)

The limited fossil record of enteropneust hemichordates (acorn worms) and the few external features that distinguish the four families have provided a challenge to our understanding of the evolution of the group and their various feeding adaptations. The middle Pennsylvanian Saccoglossus testa sp. nov. from the Mazon Creek, Westfalian D Carbonate Formation, Francis Creek Shale of northern Illinois provides evidence for the exploitation of surface sediments. Saccoglossus testa has a long proboscis characteristic of the extant genus Saccoglossus, a specialist in surface deposit feeding. The collar is as long as it is wide. The anterior trunk lacks a distinctively wide branchial region. These three features distinguish it from its sympatric enteropneust species Mazoglossus ramsdelli Bardack that has a proboscis characteristic of an infaunal deposit feeder. It is the seventh known species of fossil enteropneust, including a resting trace of a Lower Triassic fossil that has collar lips that characterize the extant deep‐sea family Torquaratoridae, and which represents a second parallel evolution of surface deposit feeding. An analysis of the seven fossils shows that the earliest Enteropneusta had a relatively simple harrimaniid‐like body plan, and that the spengelid, the torquaratorid and lastly the most complex ptychoderid body plan appeared in that chronological order.     

Fine structure of eyespots in tornarian larvae (Phylum: Hemichordata)

Summary The eyespots of tornariae of enteropneusts (Ptychodera flava from Hawaiian waters and an unknown species from southern California) were studied by electron microscopy. An ocellus is composed of two types of cells: sensory and supportive. The former is characterized by a bulbous cilium (with 9+2 axoneme) at its distal end, one or sometimes two arrays of microvilli from its sides below the cilium, and a basal axon. The latter features large, clear vesicles which presumably contained the reddish-orange pigment seen in the ocellus of a living larva. Five-day old tornariae of P. flava are positively phototactic. Both cilium and microvilli may function as photoreceptors. The tornarian ocellus studied is compared with eyespots of other invertebrates, and the evolutionary significance of its putative photoreceptors is discussed.We acknowledge the kind assistance of Drs. Michael G. Hadfield, University of Hawaii, and Russel L. Zimmer, Santa Catalina Marine Biological Laboratory, and the support of grant 10292 from the USPHS.     

Observations on torquaratorid acorn worms (Hemichordata,Enteropneusta) from the North Atlantic with descriptions of a new genus and three new species

Enteropneusts in the family Torquaratoridae were imaged using still and video cameras in the deep North Atlantic and then collected by remotely operated vehicles. From this material, we describe Yoda purpurata n. gen, n. sp., Tergivelum cinnabarinum n. sp., and Allapasus isidis n. sp. Individuals of the first two species were browsing completely exposed on the sea floor, whereas the specimen of the last species was encountered floating ~1 m above the sea floor. Living specimens of Y. purpurata were 12–19 cm long and had a dark reddish‐purple proboscis, collar, and genital wings (folded dorsally over the anterior region of the trunk). Members of this species were hermaphrodites (the first ever discovered in the phylum Hemichordata), with numerous separate testes and ovaries in the genital wings. Living specimens of T. cinnabarinum were 12–26 cm long and had a cinnabar‐colored proboscis, collar, and back veils (arising from the anterior region of the trunk); sexes were separate, and body shape and internal morphology closely resemble those of its brown congener, T. baldwinae, from the eastern Pacific. The only specimen of A. isidis collected was a male 13 cm long and pale yellow when alive. Its body shape was proportionally shorter and broader than that of its orange congener, A. aurantiacus, from the eastern Pacific, but the internal anatomy of the two species is virtually identical. [Correction made after online publication August 21, 2012 to correct species name in preceding sentence.]     

Structure of the digestive tract of tornaria larva inEnteropneusta (Hemichordata)

The ultrastructure of the digestive tract of tornaria larva of enteropneusts was investigated. It showed that the digestive tract consists of three parts: esophagus, stomach, and intestine. The esophagus epithelium consists of two types of multiciliated epithelial cells and solitary muscle cells. Axonal tracts and neurons were found in the ventral wall of the esophagus. The cardiac sphincter contains an anterior band of strongly ciliated cells and a posterior band of cells with long vacuolized processes which partition the sphincter lumen. The stomach consists of three cell types: (1) cells with electron-opaque cytoplasm, bearing a fringed border on their apical sides; (2, 3) sparse cells with electron-light cytoplasm and different patterns of apical microvilli. Cells of the pyloric sphincter bear numerous cilia and almost no microvilli. The intestine consists of three parts. The anterior part is formed of multiciliated cells which bear the fringed border. The middle part consists of flattened cells bearing rare cilia and vast numbers of mace-like microvilli. The posterior part of the intestine is formed of cells bearing numerous cilia and few microvilli. Muscle cells were not found in either stomach or intestine epithelium. One noticed that the structure of the digestive tract of enteropneust tornaria larva differs from that of echinoid pluteus larva.     

Spermiogenesis and ultrastructure of spermatozoa in Saxipendium coronatum (Hemichordata,Enteropneusta), with consideration of their relation to reproduction and dispersal

Summary Sperm ultrastructure and spermiogenesis of the enteropneust hemichordate Saxipendium coronatum conforms to the general pattern of the prototype spermatozoon found in many phyla. The sperm is about 29 m long, including head, middle piece, and tail. The Saxipendium spermatozoon has some unique features. The head is pyramidal in shape and the nucleus has four frontal ridges radiating from the base of the acrosomal region. The acrosome is composed of a large acrosomal vesicle surrounded by periacrosomal material. The acrosomal region projects about 1 m in front of the nucleus and has a width at the base of 1.5 m. The middle piece is dish-shaped and contains a large mitochondrial mass surrounding the centriolar region. The centriolar region is partially located in a centriolar fossa at the basal part of the nucleus. In spermatids, an anchoring fiber apparatus is observed surrounding the centriolar region. The distal ends of the fibers are attached to the plasmalemma by electron-dense thickenings. The tail is a simple flagellum. The sperm of Saxipendium and the small eggs found in the female suggest non-specialized external fertilization and embryogeny leading to a planktotrophic larva. The main results of the fine structure of the spermatozoon in Saxipendium are summarized in Fig. 12.Abbreviations used in the figures an antrum - av acrosomal vesicle - ax axoneme - d distal centriole - ep epidermis - f flagellum - gp gonopore - m mitochondrion - mp middle piece - n nucleus - p proximal centriole - per periacrosomal material - sp sperm - te testis - vac vacuolated cells     

Cephalodiscus reproductive biology (Pterobranchia,Hemichordata)

Sexually mature adults and embryos and larvae of Cephalodiscus nigrescens and C. gracilis were studied by light and electron microscopy. Contrary to claims in the literature, individual coenecial cavities are inhabited by colonies of up to 15 joined zooids and not by single individuals, which is important for the interpretation of the mode of life of the related fossil group the graptolites. Some aspects of the reproductive apparatus and reproduction in Cephalodiscus are reported. The ultrastructure of the spermatozoon is described for the first time. Coelom formation is by schizocoely. The structure of the larva at several developmental stages is illustrated. Not all fertilised eggs are destined to become motile larvae and some develop into zooids omitting the motile stage. The lumen of the oviduct is much larger than previously supposed. Spermatozoa are shed into the cavity of the coenecium. It is proposed that fertilisation takes place within the coenecium. The ultrastructure of the enigmatic black ‘Comma Body’ is described and a reproductive function is proposed. Budding takes place from a base common to several zooids. This base probably also serves as an attachment foot. Large masses of yolk have been discovered within the coelom of some zooids and muscle stalks. It is inconceivable that a colony of Cephalodiscus nigrescens could survive unless it spent most of its life outside the coenecium.