Ultrastructure and chaetotaxy of sensory receptors in the cercariae of a species of Crepidostomum Braun, 1900 and Bunodera Railliet, 1896 (Digenea: Allocreadiidae)

Previous investigations of cercarial sensory systems have focused on chaetotaxy and ultrastructure of sensory receptors and have revealed chaetotaxic patterns within families, genera, and species as well as different types of sensory receptors. However, chaetotaxic and ultrastructural observations have rarely been combined. We investigated the ultrastructure of cercarial sensory receptors in conjunction with the chaetotaxy and neuromorphology in 2 allocreadiid species belonging to the genera Crepidostomum and Bunodera. Cercariae were treated with acetylthiocholine iodide and silver nitrate, and for scanning electron microscopy (SEM) and transmission electron microscopy (TEM). Similar cholinergic nerve networks were revealed. Chaetotaxy was consistent with that of other allocreadiids. Seven and 6 types of receptors were distinguished with SEM in Crepidostomum sp. and Bunodera sp., respectively. Types differed in number of cilia (1 or 2), cilium length (short, moderately long, or long), presence or absence of a tegumentary collar and a domelike base, and tegumentary collar length (low, moderately low, or high), TEM of some types revealed unsheathed cilia, basal body, and thickened nerve collars. Some receptor types were site specific. Thus, long uniciliated receptors were concentrated on the dorsal surface. Other types, such as short uniciliated receptors, were widespread throughout most regions. Ultrastructure and site-specificity observations suggest that most receptors are mechanoreceptors.     

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.     

Head sensory organs of Halobiotus stenostomus (Eutardigrada, Hypsibiidae)

The structure and arrangement of sensory organs in the tardigrade Halobiotus stenostomus (Richters 1908) have been studied using transmission and scanning electron microscopy techniques. The sensory organs found on the head of H. stenostomus are as follows: the circumoral sensory field, cephalic papillae, anterolateral and posterolateral sensory fields, and suboral sensory region. Four types of ciliated receptor structures are described in the sensory fields. The lateral sensory fields contain two types of receptor endings, dense and lucent, which differ in the presence or absence of a collar and in the structure of the outer dendrite segment. Two more types of receptor endings, ultrastructurally differing from the lateral sensory field receptors, are located in the suboral sensory region. Receptors with an asymmetric collar have been found, and a receptor ending without a collar is described for the first time in tardigrades. Unlike in other species studied, the sensory organs of H. stenostomus lack the lymph cavity surrounding the outer receptor segment. Similarity and differences in the ultrastructure of receptors between H. stenostomus and other species of Eutardigrada and Heterotardigrada are discussed.     

The Nervous System of the Male Dinophilus gyrociliatus (Annelida: Polychaeta). I. Number, Types and Distribution Pattern of Sensory Cells

The entire nervous system of the smallest annelid hitherto known, the dwarf male of the highly dimorphic species Dinophilus gyrociliatus , has been reconstructed by means of TEM investigations of serial ultrathin sections. Altogether there are 68 neurons, 40 of which have a sensory function. The structure and distribution of them is described. The receptor endings of the 20 sensory cells of each side are located either in two groups — the anterior receptor group and the posterior receptor group — or are singly positioned in the integument. Structural differences of the apical portion of the dendrites enables four types of receptors to be distinguished: three types with emergent cilia and one type with non-emergent cilia. Neurons with emergent cilia can be monociliated collar cells as well as mono- or multiciliated cells without collar. Special vesicle-in-vesicle structures, are located close to the basal portion of the cilia in some of these cells. The non-emergent cilia border closely to a neighbouring epidermal cell and contain a prominent intraciliary vesicle. The function of receptors is discussed with regard to a comparison with receptors in other polychaete species, structural specializations and their distribution pattern on the animal's surface.     

Topography and ultrastructure of the tegument of Lecithochirium musculus (digenea: Hemiuridae), a parasite of the European eel Anguilla anguilla (osteichthyes: Anguillidae)

The tegumental ultrastructure of the stomach fluke Lecithochirium musculus was studied using scanning and transmission electron microscopy. The surface of the tegument was smooth and covered by transverse cytoplasmic ridges. Cobblestone‐like units of the tegument were observed on the ventral surface. Invagination and evagination of the ecsoma induced variations in the tegumental surface. The ultrastructural study revealed that the tegument of L. musculus had a typical syncytial organization with a distal cytoplasm lying over a basal matrix and cytons. Two types of intra‐tegumental sensory structures were observed. Type 1 sensory receptor was a domed‐like fusiform structure consisting of a smooth elevation of the tegument. Four receptors of this type were observed on the anterior dorsal surface of the fluke. Three nerve bulbs filled with electron‐lucent material and mitochondria composed this receptor. Hemispherical electron‐dense collars were observed at the top of the nerve bulbs. Striated rootlets laid just beneath the hemispherical electron‐dense collars. Type 2 sensory receptor presented two morphological variations, i.e., a bulb‐like monolobed structure, and a bulb‐like bilobed structure observed at two different degrees of evagination. For both variations, the nerve bulb enclosed mitochondria, electron‐lucent material, and a conical electron‐dense collar from which extended a striated rootlet. Numerous sensory receptors of this type were observed around the ventral sucker. J. Morphol., 2012. © 2011 Wiley Periodicals, Inc.     

Innervation of cercarial tegumentary receptors investigated by the Sevier-Munger method

The investigation of the sensory nature of tegumentary receptors in platyhelminths remains a challenge due to technical difficulties related to nerve tissue exposure and its experimental handling. Neuromorphological studies have been carried out but few demonstrated the association of these receptors with the nervous system. This paper introduces the Sevier-Munger method as an alternative approach to study the innervation of tegumentary receptors in larval flatworms. Twenty heterophyid cercariae were fixed in hot 5% formalin, with all washes performed in tap and distilled water. They were developed in a solution of ammoniacal silver and 2% formalin under the microscope for 10 min, with preparations shaken gently throughout the procedure. In all specimens, nerve cells stained black against a pale gold background. Fine nerve fibers of the subsurface nerve plexus were observed. These fibers sent distal branches from the plexus to the cercarial tegument. The branches became fine nerve endings, projecting as receptors in the cephalic (5CIV₅, 2CV₂, and 2CV₄), anterior (4AIL, 3AIIL, 2AIIIL), midbody (1ML, 3MV), posterior (1PIL, 1PIIL, and 1PIIIL), and caudal (2UD) regions of the cercaria. These results indicate that the Sevier-Munger method is useful to demonstrate the association of cercarial tegumentary receptors with the subsurface nerve plexus. They also recommend the use of alternative methods to further investigate flatworm nervous systems. Moreover, there is a pressing urge for a standardized protocol, combining a plethora of methods and techniques. Interdisciplinary collaboration aiming at a better understanding of the function of flatworm nervous systems is particularly encouraged.     

Observations on cercarial chaetotaxy as a means for the identification of European species of Trichobilharzia Skrjabin & Zakharow, 1920 (Digenea: Schistosomatidae)

In order to evaluate the importance of cercarial chaetotaxy in the identification of European avian schistosomatids of the genus Trichobilharzia Skrjabin & Zakharow, 1920, papillary patterns of T. franki Müller & Kimmig, 1994 and T. ocellata (La Valette, 1855) Brumpt, 1931 were examined and compared. Scanning electron microscopy (SEM) was also employed to confirm the number and distribution of the sensory papillae. The chaetotaxy of T. franki and T. ocellata were identical, which suggests a close kinship between the two species. Some sensory papillae stained insufficiently with silver nitrate or were difficult to examine using light microscopy. Thus, the use of SEM in future examinations of Trichobilharzia chaetotaxy will ensure the collection of data that are comparable between studies, even though some argentophilic structures are not visible using SEM.     

日本棘隙吸虫体被超微结构的研究

本文报道扫描电镜观察下日本棘隙吸虫皮式、体棘和3种感觉乳突的形态和分布。     

The sensory epithelium of the tentacles and the rhinophore of Nautilus pompilius L. (cephalopoda, nautiloidea)

Nine intraepithelial ciliated cell types that are presumed to be sensory cells were identified in the epithelium of the pre- and postocular tentacles, the digital tentacles, and the rhinophore of the juvenile tetrabranchiate cephalopod Nautilus pompilius L. The morphological diversity and specialization in distribution of the different ciliated cell types analyzed by SEM methods suggest that these cells include receptors of several sensory functions. Ciliated cell types in different organs that show similar surface features were combined in named groups. The most striking cell, type I, is characterized by a tuft of long and numerous cilia. The highest density of this cell type occurs in ciliary fields in the epithelium of the lamellae of the pre- and postocular tentacles, in the olfactory pits of the rhinophores, and in the lamellae of four pairs of lateral digital tentacles, but not in the epithelium of the medial digital tentacles. The similar morphological data, together with behavioral observations on feeding habits, suggest that this cell type may serve in long-distance chemosensory function. The other ciliated cell types are solitary cells with specific spatial distributions in the various organs. Cell types with tufts of relatively short, stiff cilia (types III, IV, VIII), which are distributed in the lateral and aboral areas of the tentacles and at the base of the tentacle-like process of the rhinophore, are considered to be employed in mechanosensory transduction, while the solitary cells with bristle-like cilia at the margin of the ciliary fields (type II) and at the base of the rhinophore (type IX) may be involved in chemoreception. Histological investigation of the epithelium and the nerve structures of the different organs shows the proportion and distribution of the sensory pathways. Two different types of digital tentacles can be distinguished according to their putative functions: lateral slender digital tentacles in four pairs, of which the lowermost are the so-called long digital tentacles, participate in distance chemoreception, and the medial digital tentacles, whose terminal axial nerve cord may represent a specialized neuromechanosensory structure, appear to have contact chemoreceptive abilities.     

Scanning electron microscopy of Echinostoma revolutum (Trematoda) during development in the chick embryo and the domestic chick

Fried B. and Fujino T. 1984. Scanning electron microscopy of Echinostoma revolutum (Trematoda) during development in the chick embryo and the domestic chick. International Journal for Parasitology14: 75–81. Scanning electron microscopy (SEM) was used to study the development of chemically excysted metacercariae of Echinostoma revolutum on the chick chorioallantois. SEM studies were also made on preovigerous adults of E. revolutum grown in the domestic chick. During worm development on the chorioallantois the tegument changed from smooth to granular and sensory papillae on the suckers became well-defined. As worms developed on the chorioallantois the cephalic collar spines became thicker and more curved and the tegumentary spines showed marked changes in shape, size and distribution on both ventral and dorsal aspects of the body. Changes in the surface ultrastructure of worms grown on the chorioallantois were essentially similar to those observed in preovigerous worms from chicks.     

Functional topography and ultrastructure of periarticular mechanoreceptors in the lateral elbow region of the rat

The distribution and ultrastructure of sensory nerve endings were investigated in the deep lateral elbow region of the rat. Three zones of distribution of mechanoreceptors were distinguished, each in relation to the functional architecture of the connective and muscular tissue in that area: (1) a zone with muscle spindles, Golgi tendon organs, free nerve endings and single small lamellated corpuscles ('muscle-tendon spectrum'), situated in the middle third of the supinator muscle and its superficial aponeurosis; (2) a zone with small lamellated corpuscles and free nerve endings, situated pericapsularly to the humeroradial joint capsule ('shearing spectrum'): this moderately dense, irregular connective tissue is covered by the proximal continuation of the supinator's aponeurosis, and muscle fibers insert from beneath this aponeurosis, which displays, as a part of the joint capsule, a strong collagenous tissue plate; (3) a zone with only free nerve endings within the tendon-like, most proximal part of the supinator's aponeurosis, inserting into the periosteal layer of the lateral humeral epicondyle ('endotenonial spectrum'): it is part of the joint capsule. The ultrastructure of these sensory endings is described and the distribution pattern of the mechanoreceptors observed is discussed in relation to the classification into 'muscle receptors' and 'joint receptors'.     

Comparative study of sensilla and other tegumentary structures of Myrmeleontidae larvae (Insecta,Neuroptera)

Antlion larvae have a complex tegumentary sensorial equipment. The sensilla and other kinds of larval tegumentary structures have been studied in 29 species of 18 genera within family Myrmeleontidae, all of them with certain degree of psammophilous lifestyle. The adaptations for such lifestyle are probably related to the evolutionary success of this lineage within Neuroptera. We identified eight types of sensory structures, six types of sensilla (excluding typical long bristles) and two other specialized tegumentary structures. Both sensilla and other types of structures that have been observed using scanning electron microscopy show similar patterns in terms of occurrence and density in all the studied species (with few exceptions). The sensilla identified are: coeloconica, placoidea, basiconica, trichodea type I, trichodea type II, and campaniformia. All these sensilla have mechano- or chemosensorial functions. Some regions of the larval body have been studied using SEM for the first time, such as the surface of the food canal, which bears sensilla coeloconica, and the abdominal segment X, that bears three types of sensilla: coeloconica, basiconica, and campaniformia. Sensilla placodea are newly reported on antlion larvae, being present on the mandibular base, pronotum, mentum, and cardum. Also, new locations of sensilla coeloconica (e.g., on rastra) and sensilla campaniformia (e.g., on odontoid processes) are noted. A novel porous texture with chemoreceptor function has been identified in the base of mandibles. A mechanism of dentate-notched surfaces that anchor maxillae and mandible, reinforcing the food canal, is detailed. All these sensorial structures, in addition to ocular tubercles for light caption and their great muscular system, confer to these larvae an extraordinary predation capacity to success hunting and living in such harsh environments.     

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.     

Monociliary receptors in interstitial Proseriata and Neorhabdocoela (Turbellaria Neoophora)

Summary The ultrastructure of monociliary receptors in 10 species of the Proseriata and Neorhabdocoela is described, with particular reference to the epidermal dendritic part.Sensory cells with a single kinocilium situated at the level of the distal epidermis membrane are considered as mechano- or chemoreceptors.There exist sensory cells with a dendrite penetrating one epidermis cell and bearing an embedded kinocilium and a collar of 8 stereocilia or ridges with a fribrillose substructure. These collared receptors probably function as mechanoreceptors.In comparison with collared sensory cells in species of other turbellarian orders, the embedded receptors in the Proseriata and Neorhabdocoela are more advanced and possess synapomorphous characteristics. With the embedded receptors a new evidence is given for the close phylogenetic relationship between the Proseriata and Neorhabdocoela.The distribution of collared cells in the animal system and their phylogenetic implication for a choanoflagellate origin of the Metazoa are briefly discussed.List of abbreviations ar annular rootlet - bm basement membrane - cb crystalline body - cc collar cell - cw cell web - cwt cell web-thickening - d dendrite - kc kinocilium - lm longitudinal musculature - mv microvilli - n nerve - nt neurotubuli - pb parenchymal branches - r rootlet - rd ridges - rh rhabdite - rm ring musculature - sc stereocilia - sd septate desmosomes - tm transversal musculature - u ultrarhabdites - za zonula adhaerens     

Ring-shaped organization of cytoskeletal F-actin associated with surface sensory receptors of Schistosoma mansoni: a confocal and electron microscopic study

The surface syncytial epithelium of the human blood fluke, Schistosoma mansoni, contains numerous ciliated or unciliated, bulb-shaped sensory receptors. At the ultrastructure level, sensory receptors with similar topographic and morphological structures have been found in the epithelial surface layers of all known species of schistosomes and other species of flatworm parasites. Although many studies have focused on the syncytial cytoskeleton of schistosomes, while some other studies have examined the fine structures of the syncytial sensory receptors, no-one has demonstrated the association of cytoskeletal elements with the surface sensory cells except the well-known microtubules associated with ciliated structures. The present study, using confocal laser scanning microscopy combined with scanning and transmission electron microscopies, demonstrates the association of ring-shaped F-actin within the epithelial sensory receptors. The F-actin rings can be characterized into two types according to their size, density, and distribution. The actin rings found in the syncytia of both the male and female schistosomes appear to be more dense and larger in size than the actin rings located only at the central regions of the tuberculated structures of the male dorsal syncytium. Our observation of F-actin rings associated with the spine-bearing tubercles, combined with the results obtained from other ultrastructural investigations, also indicate the presence of the unciliated sensory receptors in each tuberculated structure of the male dorsal surface syncytium, which have not been reported in other studies on schistosome epithelial sensory cells.     

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.     

纤细背孔吸虫体被超微结构的研究

本文对人工感染获得的纤细背孔吸虫Notocotylus attenuatus(Rud.,1809)成虫的体被进行了扫描电镜观察。发现虫体不同部位的体被有着不同的被式。口吸盘处为放射状条索;虫体腹面口吸盘后至中列第一腹腺前为无棘区,呈石板条块状,其余部分均为银杏叶和尖叶形体棘所覆盖。虫体背面边缘一圈为有棘区,其圈内为珠状突起结构。     

Sensory cells in the sucker of Craspedella pedum (Plathelminthes, Temnocephalida): in vivo staining with DiO and SEM and TEM observations

 Two pairs of identified sensory neurons innervating the sucker of Craspedella pedum (designated ADS1, ADS2) were found to accumulate DiO (3,3′-dioctadecyloxacarbocyanine perchlorate) in vivo. The number, position and morphology of these neurons do not change throughout the postembryonic period of life. The axons of the ADS cells run forward within the ventral cords and their dendrites are parallel. They enter the sucker, ramify and terminate in numerous sensory endings in a wide peripheral zone of the disc. SEM reveals a single type of sensilla: small spot-like structures with several short cilia. They are scattered within the zone accommodating the openings of the adhesive glands and their distribution corresponds to that of the stained terminals. TEM observations (including about 20 full reconstructions from serial ultrathin sections) show five types of sensory endings on the disc with the following structures: (1) a short cilium and thin rootlet, (2) aciliary with a normal rootlet and a club-shaped apical portion, (3) aciliary with a club-shaped apical portion and a body similar to the apical part of the rootlet, (4) aciliary with large apical granule and (5) aciliary with small apical granules. Type 2–5 receptors form a morphological series suggesting that they are stages of formation of the common type 4 receptor. Not fully formed type 1 receptors have been found within the epidermis in adult animals. This suggests that, although ADS perikarya persist throughout the life of the animal, the nerve endings they form might be constantly renewed. Judging from the morphological and behavioural data, the functions of the ADS neurons might include: (1) monitoring of the close contact between the surface of the sucker and the substratum prior to adhesion and (2) checking the viscosity of the adhesive secretion prior to release of the sucker. Accepted: 16 December 1997     

Sensory receptors of the miracidium of Gigantocotyle explanatum (Trematoda:Paramphistomidae)

Five types of sensory receptors are described. Both uniciliated and multiciliated nerve endings occur on the apical papilla. The former structures possibly have a tango- or rheo-receptive function, while the latter may have a chemoreceptive function. A number of uniciliated sensory structures are also present embedded within the intercellular ridges. A pair of unciliated lateral papillae are located in the intercellular ridge separating the first and second tiers of epidermal cells. Each is associated with a number of sheathed unciliate nerve bulbs. A pair of internal “lamellate ciliary organs” are ascribed a photoreceptive function. Each comprises a cylindrical cell body enclosing a large cavity, into which project eight or more cilia bearing a number of concentrically arranged spherical lamellae. A single unicellular “conical organ”, covered with microvilli, projects into an extracellular space, bounded in part by the lateral glands. This structure may represent a second type of photoreceptor, or alternatively may serve as a gyroscopic device.