Ultrastructure of the sense receptors of adult Multicotyle purvisi (Trematoda, Aspidogastrea)

The following presumptive sense receptors of adult Multicotyle purvisi from the intestine of freshwater turtles in Malaya are described by transmission electron microscopy: disc-like receptor with many electron-dense collars and modified ciliary rootlet forming a 'disc'; non-ciliate receptor with long rootlet; non-ciliate receptor with branching rootlet and dense mass of irregularly arranged microtubules; non-ciliate receptor with rootlet fanning out from basal body, cross-striated in its upper and with electron-dense structures in its lower part; uniciliate receptor with thick layer of cytoplasm around axoneme; receptor with short cilium, at base of deep invagination of tegument; receptor with short cilium terminating in an electron-dense apical cap; and uniciliate receptor with long cilium. In addition, there may be a small non-ciliate receptor with a long ciliary rootlet at the base of the thick dorsal tegument, and uniciliate receptors differing from the uniciliate receptor with long cilium in the number of electron-dense collars and the length of the cilium and ciliary rootlet. Implications of the findings for the phylogeny of the parasitic Platyhelminthes and for evolutionary trends within that group arc discussed. The considerable degree of divergence of receptor types between the species of one family is attributed to the archaic nature of the group.     

Ultrastructure of the abdominal sense organ of the scallop <Emphasis Type="Italic">Mizuchopecten yessoensis</Emphasis> (Jay)

The sensory epithelium of the abdominal sense organ (ASO) of the scallop Mizuchopecten yessoensis is composed of three cell types, sensory cells, mucous cells, and multiciliated cells. Sensory cells bear a single long (up to 250 microm) cilium surrounded by an inner ring of nine modified microvilli and an outer ring of ordinary microvilli paired with modified microvilli. Sensory cells make up about 90% of the total number of cells in the sensory epithelium. Mucous cells, which are much wider than sensory cells, bear only ordinary microvilli on their apical surface. Rare multiciliated cells with short (4-6 microm) cilia are scattered in the periphery of the sensory epithelium sheet. All hairs, cilium, and microvilli of each sensory cell are interconnected by a fibrous network. Nine modified microvilli of a single cell are interconnected by prominent laterally running fibrous links. Membrane-associated electron-dense material of modified microvilli is connected to the ciliary membrane-associated electron-dense material by fine string-like links. These links mechanically bridge the space between the cilium and modified microvilli, as do mechanical links, described for the stereocilia and kinocilium of vertebrate vestibular and cochlear hair cells. The proximal portion of a sensory cilium is about 100 microm long and has a typical 9 x 2+2 axoneme arrangement. The distal portion of a cilium is approximately 2 times thinner than the proximal one and is filled with homogeneous electron-dense material. Along the distal portion, diffuse material associated with the external surface of the membrane is found. The rigidity of distal portion of a cilium is much less than that of the proximal one.     

Correlation of fluorescence and electron microscopy of F-actin-containing sensory cells in the epidermis of Convoluta pulchra (Platyhelminthes: Acoela)

Phalloidin‐stained whole mounts of acoel turbellarians show brightly fluorescing club‐shaped structures distributed over the epidermis and concentrated especially at the anterior and posterior tips of the body. By correlating electron micrographic images and fluorescence images of Convoluta pulchra, these structures can be seen to be sensory receptors with a central cilium surrounded by a collar of microvilli. The other candidate for showing fluorescence in the epidermis, namely gland necks, can be ruled out since their distribution is too dense to resemble the distribution of the fluorescent structures seen here. The collared sensory receptors were inserted between epidermal cells, and each bore a central cilium surrounded by a collar of 6–18 microvilli and an additional centrally positioned 2–7 microvilli of which 2 or 3 were associated with a modified rootlet called the swallow’s nest. Confocal scanning laser microscopy resolved the core of actin filaments within the microvilli of the collar and their rootlet‐like connections to the base of the sensory cell. Such receptors could also be identified by fluorescence microscopy in several other species of acoel turbellarians.     

Sensory and secretory cells ofOphryotrocha puerilis (Polychaeta)

Summary As revealed by glyoxylic acid induced fluorescence, the protandric polychaeteOphryotrocha puerilis possesses different types of catecholaminergic primary bipolar sensory cells, the perikarya of which are located beneath the epidermis. About 20 of such receptors are situated in each segment but they are mostly found on antennae, palps, urites and parapodial cirri. The dendrites of these sensory neurones run to the cuticle and dilate to form receptive endings. Three different types of dendritic endings could be distinguished: (1) multiciliary receptors with 4–8 cilia and ciliary rootlets, (2) monociliary receptors with microvilli arranged like a funnel and electron-dense cuffs and (3) monociliary receptors of the collar-type with, constantly, ten microvilli surrounding one single central cilium. The latter type is also characterized by rootlet fragments. Dendrites and dilated receptive endings of all three types contain clear (putative secretory) vesicles, multivesicular bodies and mitochondria. Pharmacological treatment (dopamine, reserpine) does not affect the number of secretory vesicles of the receptor neurones. Extra vesicular storage of catecholamines is discussed. Secretory cells of unknown function containing large numbers of electron-dense vesicles are usually found in close association with sensory cells.Abbreviations CA catecholamines - DA dopamine - RE reserpine     

Ultrastructure of the water-movement-sensitive sensilla in the medicinal leech

Behavioral and physiological experiments have shown that medicinal leeches are able to detect low amplitude surface waves, and further, that the transduction of this stimulus modality occurs primarily, if not exclusively, at the annular sensilla (Young, Dedwylder, and Friesen, 1981; Friesen, 1981). Here we examine the morphology of these specialized sensory structures using light, scanning electron, and transmission electron microscopes. We found that three types of ciliated sensory cells occur at the sensilla: (1) a uniciliate cell, with an axial cilium that projects at least 12 μm beyond the cuticle; (2) a multiciliate cell with from two to four grouped cilia that extend 1–3 μm beyond the cuticle; and (3) a second multiciliate cell, whose cilia project parallel to the body surface but remain within the cuticle. The cilia of all three cell types arise from the cuplike depressions which form the apices of slender, elongated cells (approximately 2 μm diameter × 50 μm length). A complexly interconnected ring of microvilli surrounds the cilium of the uniciliate cells. The morphology of the uniciliate cells closely resembles the structure of vibration-sensitive sensory neurons found in other species. We propose, based on previous results and our new findings, that the uniciliate receptor cells are the sensillar movement receptors which mediate leech sensitivity to water movements.     

Ciliated sensory receptors of the unactivated metacestode of Hymenolepis microstoma

The fine structure of the ciliated sensory endings of the unactivated metacestode of Hymenolepis microstoma is described. The type I sensilla, localized in areas of the scolex and sucker tegument, are characterized by a long cilium (1.20 × 0.20 μ) embedded in a bulb containing two electron-dense collars and three to five mitochondria. The type II sensilla, located in tegumentary pits of the rostellum, are characterized by a short cilium (0.62 × 0.28 μ) possessing ciliary rootlets, embedded in a bulb containing a single electron-dense collar and one to three mitochondria. Both sensory cilia are characterized by a 9 + 6 + 1 microtubular substructure. The sensory bulbs contain large numbers of membrane bound electron-lucent vesicles; neurotubules are absent at this stage of development.     

Ultrastructure of multiciliated collar cells in the pilidium larva of Lineus bilineatus (Nemertini)

Summary The ultrastructure of the apical plate of the free-swimming pilidium larva of Lineus bilineatus (Renier 1804) is described with particular reference to the multiciliated collar cells. In the multiciliary collar cells there are several, up to 12, cilia surrounded by a collar of about 20 microvilli extending from the cells' apical surface. The cilia have the typical 9+2 axoneme arrangement and are equipped with striated caudal rootlets extending from the basal bodies. No accessary centriole or rostral rootlet were observed. Microvilli surrounding the cilia are joined in a cylindrical manner by a mucus-like substance to form a collar. In comparison with many sensory receptor cells built on a collar cell plan the multiciliary collar cells of the pilidium larva apical plate are rather simple and unspecialized. In other pilidium larvae monociliated collar cells are found in the apical plate. The possible function and phylogenetic implications of multiciliated collar cells in Nemertini are briefly discussed.List of Abbreviations a axoneme - b basal body - c cilia or flagella - d desmosome - G Golgi apparatus - m mitochondria - mf microfilaments - mu mucus - mv microvilli - n nucleus - nt neurotubules - pm plasma membrane - r rootlet - ri ribosomes - v secretory vesicles     

Ultrastructural study of sensory cells of the proboscidial glandular epithelium of Riseriellus occultus (Nemertea,Heteronemertea)

Only one sensory cell type has been observed within the glandular epithelium of the proboscis in the heteronemertine Riseriellus occultus. These bipolar cells are abundant and scattered singly throughout the proboscis length. The apical surface of each dendrite bears a single cilium enclosed by a ring of six to eight prominent microvilli. The cilium has the typical 9×2 + 2 axoneme arrangement and is equipped with a cross-striated vertical rootlet extending from the basal body. No accessory centriole or horizontal rootlet was observed. Large, modified microvilli (stereovilli) surrounding the cilium are joined together by a system of fine filaments derived from the glycocalyx. Each microvillus contains a bundle of actin-like filaments which anchor on the indented inner surface of a dense, apical ring situated beneath the level of the ciliary basal body. The tip of the cilium is expanded and modified to form a bulb-like structure which lies above the level where the surrounding microvilli terminate. In the region where the cilium emerges from the microvillar cone, the membrane of the microvillar apices makes contact with a corresponding portion of the ciliary membrane. At this level microvilli and cilium are apparently firmly linked by junctional systems resembling adherens junctions. The results suggest that these sensory cells may be mechanoreceptors. © 1996 Wiley-Liss, Inc.     

Ultrastructural studies of epidermis, sense receptors and sperm of Craspedella sp. and Didymorchis sp. (Platyhelminthes, Rhabdocoela)

Craspedella has a non-ciliated epidermis with nuclei located in the epidermis and with short microvilli. There is a thin basal lamina and thick underlying fibrous matrix. Rhabdites are secreted through ducts lined by microtubules. Multiciliate sense receptors consist of bundles of dendrites in a depression of the epidermis. Each dendrite has a cilium with a cross-striated rootlet; there are no electron-dense collars. Spermatozoa have peripheral microtubules which in cross-section are arranged in a ring-like or spiral fashion, numerous electron-dense granules, mitochondria and a nucleus; axonemes of the 9 +'1'type are free for most of their length. Centrioles occur in some nerve fibres. In Didymorchis parts of the epidermis are ciliated and epidermal perikarya are 'insunk', connected to the surface part of the epidermis by a single cytoplasmic process. Epidermal cilia have cross-striated vertical and horizontal rootlets. In the ciliary tips a short electron-dense rod along the central pair of tubules extends to the tip, where it widens to become a terminal plate; peripheral doublets gradually disappear by losing their microtubules. Receptors observed are uniciliate. Spermatozoa are as in Craspedella . Ultrastructural evidence indicates that Craspedella and Didymorchis arc closely related and belong to the Rhabdocoela.     

Ultrastructure of the nerve cells and sensilla of Geocentrophora baltica (Platyhelminthes,Lecithoepitheliata) and the surface sensilla in the Geocentrophora group

Two types of nerve cell could be distinguished ultrastructurally in the central nervous system of Geocentrophora baltica (Prorhynchida, Lecithoepitheliata). Both show invaginations in the plasma membrane, but they differ in the character of the cytoplasm (light or densely stained) and the distribution of the neuronal vesicles (evenly or in groups). Different kinds of vesicles and neuronal release sites are observed. Special features of the synapses are pronounced local thickenings of the presynaptic membrane connected to paramembranous densities. In G. baltica and five endemic Geocentrophora spp. from Lake Baikal six types of surface sensillum were observed at the epidermal surface: 1. those with a long thin rootlet; 2. a short, balloon-shaped cilium with an aberrant axoneme and a reduced rootlet; 3. a rootlet branching into many striated bundles; 4. a thick rootlet; 5. a reduced rootlet and numerous neurotubules;and 6. collared sensilla each with one cilium in a deep pit surrounded by a collar of 11 to 12 microvilli. The variable number of microvilli in the collared sensillum is considered plesiomorphic relative to the stable number of eight microvilli known in sensilla of the Prolecithophora, Proseriata, and Rhabdocoela. The ultrastructure of the collar sensillum indicates that the Lecithoepitheliata is only distantly related to the Prolecithophora and higher turbellarians.     

Fine structural studies of the nervous system and the apical organ in the planula larva of the sea anemone Anthopleura elegantissima

The nervous system of the planula larva of Anthopleura elegantissima consists of an apical organ, one type of endodermal receptor cell, two types of ectodermal receptor cells, central neurons and nerve plexus. Both interneural and neuromuscular synapses are found in the nerve plexus. The apical organ is a collection of about 100 long, columnar cells each bearing a long cilium and a collar of about 10 microvilli. The cilia of the apical organ are twisted together to form an apical tuft. The ciliary rootlets of the apical organ cells are extremely long, reaching to the basal processes of the cells adjacent to the mesoglea. All three types of sensory cells are tall and slender in profile and are identified by the presence of one or more of the following features: microtubules, small vesicles, membrane-bound granules and synapses. The interneurons are bipolar cells with somas restricted to the aboral end, adjacent to the apical organ. All synapses observed are polarized or asymmetrical. A diagram including all the elements of the nervous system is presented and the possible functions of the nervous system are discussed in relation to larval behavior.     

Chaetotaxy and ultrastructure of sensory receptors in the cercaria of a species of Allassogonoporus Olivier, 1938 (Digenea:Lecithodendriidae)

A standard procedure that combines chaetotaxic, ultrastructural and neuromorphological observations has recently provided a new perspective to the study of cercarial sensory systems. In the present work, we aimed to extend the use of this combination of techniques to investigate the chaetotaxy of Allassogonoporus sp. in conjunction with the ultrastructure of sensory receptors and neuromorphology. Five nerve regions were distinguished. A conspicuous bilobed cerebral ganglion was observed at the level of the pharynx. The chaetotaxic pattern was generally consistent with that of other lecithodendriids. Four types of receptors were distinguished with scanning electron microscopy. These types differed in cilium length (short, moderately long or long) and tegumentary collar length (moderately low or high). Internal ultrastructure of receptor type IIAL revealed an unsheathed cilium, a closed basal body, septate extracellular junctional complexes and thickened nerve collars. Some receptor types were site-specific. Long uniciliated receptors were found mainly on the dorsal surface, whereas short uniciliated receptors were widespread across the tegument. Ultrastructure and site-specificity observations suggest that most sensory receptors are mechanoreceptors, probably reflecting the important role mechanoreception plays in host finding.     

Description and surface topography of the cercaria of Austrobilharzia sp. (Digenea: Schistosomatidae)

The cercaria of Austrobilharzia sp. from the marine prosobranch gastropod Planaxis sulcatus in Kuwait Bay is described. The surface microtopography and pattern of the tegumentary sensory receptors are examined using scanning electron microscopy. The general microtopography of the surface of the cercaria is similar to that previously observed in cercariae of mammalian schistosomes, although differences are recorded in the types, numbers and distribution of the sensory receptors. The study identified more than 13 types of receptors comprising aciliated, uniciliated and for the first time a multiciliated receptor in a strigeid cercaria. The ciliated receptor types differ in the cilium length and structure of the surrounding collar and tegumentary base. The receptor types are site specific: (1) the aciliated and pitlike on the anterior organ-neck region and ventral sucker; (2) the uniciliated with a long flexible cilium with or without collar or a tegumentary base on the body and tail; and (3) the uniciliated with a short rigid cilium and a robust collar and tegumentary base, and the multiciliated with 6 flexible cilia and a high cylindrical collar on the anterior organ tip. The reported SEM information on the sensory receptors may contribute to elucidating their functional role and to establishing morphological characters for the phylogeny of the family Schistosomatidae.     

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.     

A reexamination of the epithelial sensory cells of amphioxus (Branchiostoma)

The rostral epithelium of a newly metamorphosed juvenile of Branchiostoma floridae was examined at the EM level to confirm previous reports on its sensory cells. The majority of the sensory cells are of three types: two type I variants, with simple collars of unbranched microvilli surrounding their cilia, and one kind of type II cell, with an extended collar of repeatedly branched microvilli. The two type I variants differ in the structure and arrangement of the microvilli, basal body and rootlet, and the length of the cilium. Both variants are probably primary sensory cells (i.e. each has its own axon), but the data supporting this conclusion are much better for one variant than for the other. Type II cells are secondary sensory cells, with synaptic terminals borne on short extensions of the cell body. The presence of degenerating type II cells suggests that they may be subject to a regular process of loss and renewal. The results do not resolve the evolutionary issue of how amphioxus sensory cells relate to the epithelial sensory and receptor cells of vertebrates. Being primary, the type I cells resemble the supposed ancestral type more closely than do type II cells. Type II cells may be chemosensory, however, and should not be ruled out a priori as possible homologues of either primary or secondary chemosensory cells in vertebrates.     

The ciliary photoreceptor in the teleplanic veliger larvae of Smaragdia sp. and Strombus sp. (Mollusca,Gastropoda)

The cerebrally innervated eyes of the veliger larvae of Smaragdia sp. and Strombus sp. are composed of a lens, a cornea, and an everse retina. The retina contains two different types of cells, ciliary sensory cells and supportive cells which bear one or two cilia. It is suggested that: (a) the ciliary photoreceptors of these teleplanic veliger larvae are correlated with a long pelagic life in the ocean, which can last up to twelve months, and (b) that structural details of the photoreceptors can change during ontogenesis (ciliary vs rhabdomeric). Furthermore, the cilia of the supportive cells apparently tranport lens material and thus play an important role in lens formation. A decomposition mechanism of pigment granules is examined.Abbreviations bb basal body - bp basal plate - c cilium - cc corneal cell - cm ciliary membranes - cw ciliary whorl - ecm extracellular matrix - gr electron-dense granules - l lens - lb lamellar body - mp membranous pieces - mt microtubules - mv microvilli - n nucleus - oc optic cavity - on optic nerve - pg pigment granule - sc sensory cell - sj septate junction - spc supportive cell - v vesicles     

The ultrastructure of the eyes in the veliger-larvae of Aporrhais sp. and Bittium reticulatum (Mollusca,Caenogastropoda)

Summary The cerebrally innervated larval eyes of Aporrhais sp. and Bittium reticulatum are investigated by means of transmission electron microscopy. Each organ consists of a pigmented cup containing an acellular lens. The cornea overlaps the anterior portion of the eye. The retina is composed of sensory cells and supportive cells. The sensory cells of Aporrhais sp. bear one cilium and in Bittium reticulatum two cilia, the ciliary membrane being folded into numerous finger-shaped evaginations. The supportive cells contain the pigment granules and most of them bear one or two cilia, the plasmalemma of which is likewise folded. It is supposed that: (a) these cilia have a transportive function for lens material and (b) that the ciliary photoreceptor of Aporrhais sp. and Bittium reticulatum is a functional adaptation to a relatively long larval period.Abbreviations bb basal body - bp basal plate - c cilium - cc corneal cell - cm ciliary membranes - cw ciliary whorl - gd Golgi dictyosomes - gm granular material - l lens - m mitochondrion - mt microtubules - mv microvilli - mvb multivesicular body - n nucleus - pb pigment border - pg pigment granule - rer rough endoplasmic reticulum - sc sensory cell - sj septate junctions - spc supportive cell     

Cytoskeletal modifications of the sensorimotor interneurons ofHydra vulgaris (Cnidaria,Hydrozoa), indicating a sensory function similar to chordotonal receptors of insects

Summary The battery mother cell complexes in the tentacles ofHydra vulgaris contain a neuronal cell known as sensorimotor interneuron that is characterized by a modified cilium lying parallel to the mesoglea. The cilium is surrounded by up to three rings of microvilli. Microvilli and cilium arise in an unusual antiparallel orientation from the opposite poles of a central cellular cavity. The lumen of this cavity communicates with the extracellular environment by way of a straight channel-like opening that is encircled by the microvillar rings. The modified cilium extends into the channel and terminates outside in the intercellular space. The wall of the cavity and the channel are stabilized by bundles of microtubules. A prominent glycocalyx interconnects all microvilli and links the innermost microvillar ring to the cilium. Within this contact region approximately 0.7 m in length the ciliary axoneme is specifically modified: all nine microtubule doublets and up to six additional microtubules are embedded in electron-dense material. The microtubule doublets are connected to the ciliary membrane by ledges of Y-shaped cross-bridging elements. These axonemal modifications resemble those known from the hydrozoan cnidocil complex or from the outer segments of insect mechanoreceptor cells. Distribution and orientation of the sensorimotor interneuron within the tentacles indicate a mechanosensory function of the cell similar to that of chordotonal receptors of insects.     

On the ultrastructure of the abdominal sense organ of the giant scallop,Placopecten magellanicus (Gmelin)

Summary The abdominal sense organ of the giant scallop, Placopecten magellanicus, is composed of two cell types. The presumed receptor cells bear a single cilium 60 to 70 m in length. The microvilli at the apices of these cells may also be modified into microvillous whorls. From eight to twelve ciliated cells are associated with a single mucous cell. The mucous cells have a much greater diameter than the ciliated cells and contain many electron-dense mucous granules. No function has yet been determined for the ciliated cells, although a number of theories are presented.This research was supported by National Research Council of Canada Operating Grant No. A-6444 to Dr. V.C. Barber. Additional support came from the Department of Biology and the School of Graduate Studies, Memorial University. Contribution no. 250 from the Marine Sciences Research Laboratory, Memorial University of Newfoundland     

The paracrystalline structure of an insect rhabdomere (Calliphora erythrocephala)

Summary By use of a modified fixation technique, the receptor cells of the compound eye of the blowfly Calliphora erythrocephala were found to contain a regular, paracrystalline array of alternating rows of hexagonally shaped microvilli. The receptor cells R1 to R6 have a cell-specific number of microvilli per row in a cross section. Every microvillus has a filament cluster connecting the axial skeleton with the microvillar membrane. This cluster is preferentially right-left oriented relative to the longitudinal axis of the microvillar array. Three adjacent microvilli are interconnected by an electron-dense substance. A mirroring technique indicated that this intermicrovillar structure consists of three subunits, although these subunits could not be conclusively demonstrated by classical densitometry or image subtraction techniques. The electron-dense substance can be seen in all cross sections of the proximal and distal parts of the microvilli. They are cylindrical structures separating the microvilli along their entire length. It is suggested that these cylindrical aggregates contain an enzymatic complex separating the rhodopsin-containing microvillar membrane into six compartments.