Ultrastructure of a possible new type of crustacean cuticular strain receptor in Carcinus maenas (crustacea,decapoda)

A hitherto unknown sensillum type, the “intracuticular sensillum” was identified on the dactyls of the walking legs of the shore crab, Carcinus maenas. Each sensillum is innervated by two sensory cells with dendrites of “scolopidial” (type I) organization. The ciliary segment of the dendrite is 5–6 μm long and contains A-tubules with an electron-dense core and dynein arm-like protuberances; the terminal segment is characterized by densely packed microtubules. The outer dendritic segments pass through the endo- and exocuticle enclosed in a dendritic sheath and a cuticulax tube (canal), which is suspended inside a slit-shaped cavity by cuticular lamellae. The dendrites and the cavity terminate in a cupola-shaped invagination of the epicuticle. External cuticular structures are lacking. Three inner and four to six outer enveloping cells are associated with each intracuticular sensillum. The innermost enveloping cell contains a large scolopale that is connected to the ciliary rootlets inside the inner dendritic segments by desmosomes. Scolopale rods are present in enveloping cell 2. Since type I dendrites and a scolopale are regarded as modality-specific structures of mechanoreceptors, and since no supracuticular endorgan is present, the intracuticular sensilla likely are sensitive to cuticular strains. The intracuticular sensilla should be regarded as analogous to insect campaniform sensilla and arachnid slit sense organs.     

Development of antennal sensilla during moulting inNeomysis integer (Leach) (Crustacea,Mysidacea)

Summary The sensilla are associated with 6 enveloping cells. The innermost enveloping cell (e 1) secretes the dendritic sheath (=thecogen cell). All other enveloping cells are involved in the formation of the outer cuticular apparatus in secreting the cuticle of a definite region of the new hair shaft.The development of the new sensilla begins when an exuvial space expands between old cuticle and epithelium. The newly forming hair shafts lie folded back in an invagination of the epidermal tissue. Only a distal shaft part projects into the free exuvial space. The cuticle of the distal and middle shaft region is secreted by the three middle enveloping cells (e 2–e 4) (=trichogen cells), which are arranged around the dendritic sheath.The wall of the cylinder, in which the distal shaft is situated, is formed by the cuticle of the future proximal shaft region. It is secreted by the outer enveloping cells (e 5 and e 6). Furthermore, both enveloping cells form the hair socket (=trichogen-tormogen cells).The outer dendritic segments encased within a dendritic sheath run up through the newly formed hair shaft and continue to the old cuticular apparatus. The connection between sensory cells and old hair shaft is maintained until ecdysis. On ecdysis the old cuticle is shed and the newly formed shaft of the sensillum is everted like the invaginated finger of a glove. The dendritic sheath and the outer dendritic segments break off at the tip of the new hair shaft. Morphologically this moulting process ensures that the sensitivity of the receptors is maintained until ecdysis.The internal organization of the sensory cells shows no striking changes during the moulting cycle. An increased number of vesicles is accumulated distally within the inner dendritic segments and distributed throughout the outer segments of the dendrites. The cytoplasmic feature of the enveloping cells indicates that synthesis and release of substances for the cuticular apparatus of the new sensillum take place.     

The analysis of the mechanosensory origin of the infrared sensilla in Melanophila acuminata (Coeloptera; Buprestidae) adduces new insight into the transduction mechanism

The thoracic infrared (IR) sensilla of the pyrophilous jewel beetle Melanophila acuminata most likely have evolved from hair mechanoreceptors (sensilla trichodea). To further elucidate the sensory transduction mechanism, the morphology of IR sensilla and of neighbouring hair mechanoreceptors was investigated by using conventional electron microscopical techniques (SEM, TEM) in combination with focused ion beam milling (FIB). It was assumed that any deviation from the bauplan of a sensillum trichodeum is of particular concern for the transduction of IR radiation into a mechanical stimulus. Thus, the structures supposed to be relevant for stimulus uptake and transduction were homologized. Compared to a hair mechanoreceptor, an IR sensillum shows the following special features: (i) the formation of a complex cuticular sphere instead of the bristle; the sphere consists of an outer exocuticular shell as well as of an inner porous mesocuticular part. (ii) The enclosure of the dendritic tip of the mechanosensitive neuron inside the sphere in a fluid-filled inner pressure chamber which is connected with a system of microcavities and nanocanals in the mesocuticular part. Hence we propose that an IR sensillum most probably acts as a microfluidic converter of infrared radiation into an increase in internal pressure inside the sphere which is measured by the mechanosensitive neuron.     

Fine structure of the pheromone-sensitive sensilla on the antenna of the hawkmoth, Manduca sexta

The flagellar antenna of the male hawkmoth Manduca sexta carries about 42,000 pheromone-sensitive sensilla trichodea, which are arranged in 'baskets' on the single segments. Each sensillum consists of a cuticular hair up to 500 mum long and is innervated by two bipolar sensory neurons. Each neuron sends an unbranched dendrite into the hair shaft. The dendrite is subdivided by a short ciliary region into an inner and an outer segment. The inner segment is especially rich in smooth vesicles, which accumulate beneath the ciliary region where they seem to fuse with the dendritic membrane. The outer dendritic segment often shows conspicuous 'beads' along its length. Three auxiliary, or enveloping, cells belong to each adult sensillum. These are the thecogen, the trichogen, and the 'outer' cell. Most probably, the latter is not homologous with the 'traditional' tormogen cell from a genealogical point of view.     

Embryonic development and molting of the antennal coeloconic no pore- and double-walled wall pore sensilla in Locusta migratoria (Insecta,Orthopteroidea)

Summary The embryonic development of antennal coeloconic sensilla was studied at four stages between 132 and 252 h after oviposition in Locusta migratoria. Initially the anlagen of the sensilla consist of 2–4 sensory cells and 3 enveloping cells. Two additional cells contribute later to the formation of socket and pit. The dendritic outer segments of the sensory cells elongate before the trichogen process grows out (ecdysis type I) with exception of one sensory cell in anlagen of poreless (np) sensilla. Other differences between np and double-walled wall pore (dw wp) sensilla are not visible until at least about 220 h after oviposition. Molting, which was studied in four stages, follows ecdysis type I in both sensillum types. The fourth enveloping cell maintains its tight connection to the socket of the sensillum even after apolysis. Its apical portion is torn off and shed together with the old cuticle. The electron-dense material between the dendritic sheath and the cuticular wall of the peg in np sensilla, which is regarded important for stimulus transmission, is not deposited during retraction of the trichogen cell. The concentric walls and spoke channels characteristic of dw wp sensilla result from deposition of cuticular material around wedge-shaped projections of the trichogen cell. The typical trilaminar 15 nm cuticulin layer is produced only on the ridges of these sensilla. The first cuticular lining of the spoke channels is only 7 nm thick and of a different structure. A flocculent material surrounds the outgrowing trichogen process. It is continuous with the filling of the spoke channels and can thus be considered as component of the stimulus-transmitting material in the functioning intermolt dw wp sensilla.     

Moulting of mechanoreceptive hair sensilla of Lepisma saccharina (Zygentoma) and Machilis spec. (Archaeognatha)

In all insects investigated hitherto the mechanoreceptive hair sensilla possess the same organization plan. There are differences in the moulting process of hemimetabolous insects. While the functions of the three enveloping cells are corresponding, the position of the moulting porus is different. In Gryllus and Periplaneta the moulting porus is situated at the base of the hair, in Machilis 25 mum above the base of the hair. In Lepisma, however, the moulting porus is located at the tip of the hair shaft. Comparison of mechanoand contactchemoreceptive hair sensilla shows that the position of the moulting porus in primitive ectognathous insects represents an argument for the close morphological and phylogenetical relationship between both types of sensilla. Interpreting our results, the original position of the moulting porus is at the tip of the hair sensilla. In mechanoreceptors, where the moulting porus is located at the base of the hair, the original tip of the hair (position of the moulting porus) is overgrown at the side by a 'secondary hair process'.     

Apical antennal sensilla in nymphs of Libellula depressa (Odonata: Libellulidae)

Abstract. In an ultrastructural study of the apical antenna of the last nymphal stages of Libellula depressa (Odonata: Libellulidae), we found long sensilla trichodea, 2 sensory pegs, and a coeloconic sensillum on the last article of the flagellum (the distal part of the antenna). The long sensilla trichodea are mechanoreceptors, almost identical to the long filiform hairs of some terrestrial insects and the first sensilla of this kind to be described in aquatic insects. Particular attention was given to the complex coeloconic sensillum, a compound sensillum innervated by 2 groups of 3 neurons wrapped in a dendritic sheath. A cuticular sleeve envelops the distal portion of the outer dendritic segment. The cuticle of the coeloconic sensillum shows wide channels and is contiguous to the underlying granular and fibrillar layer. Similar structures on the antennae of the adults of other dragonflies were identified as chemoreceptors in previous studies. We hypothesize that this larval coeloconic sensillum might likewise have a chemosensory function, responding to molecules that diffuse through the cuticle and the underlying granular and fibrillar layer, as no clear pore or pore-tubule system is visible. Alternative functions are also explored on the basis of morphological details.     

THE FINE STRUCTURE OF COCKROACH CAMPANIFORM SENSILLA

Campaniform sensilla on cockroach legs provide a good model system for the study of mechanoreceptive sensory transduction. This paper describes the structure of campaniform sensilla on the cockroach tibia as revealed by light- and electron-microscopy. Campaniform sensilla are proprioceptive mechanoreceptors associated with the exoskeleton. The function of each sensillum centers around a single primary sense cell, a large bipolar neuron whose 40 µ-wide cell body is available for electrophysiological investigation with intracellular microelectrodes. Its axon travels to the central nervous system; its dendrite gives rise to a modified cilium which is associated with the cuticle. The tip of the 20 µ-long dendrite contains a basal body, from which arises a 9 + 0 connecting cilium. This cilium passes through a canal in the cuticle, and expands in diameter to become the sensory process, a membrane-limited bundle of 350–1000 parallel microtubules. The tip of the sensory process is firmly attached to a thin cap of exocuticle; mechanical depression of this cap, which probably occurs during walking movements, effectively stimulates the sensillum. The hypothesis is presented that the microtubules of the sensory process play an important role in mechanoelectric transduction in cockroach campaniform sensilla.     

A new mechanosensory organ on the anterior spinnerets of the spiderCupiennius salei (Araneae,Ctenidae)

We describe hitherto unknown mechanoreceptors on the anterior spinnerets of the spiderCupiennius salei. These receptors are found at the base of the spigots of the major ampullate glands which produce the dragline used by the spider as a safety thread in various behavioral situations. There are 40–60 mechanoreceptors associated with two spigots of each anterior spinneret. They are likely to provide information on the forces pulling on the dragline and also on its orientation in space. A single sensillum consists of a hole in the cuticle covered by a thin cuticular membrane. It much resembles spider slit sensilla, which are known to detect strains in the exoskeleton. Each sensillum is supplied by two dendrites most likely belonging to two bipolar sensory cells. One of the dendrites ends at the covering membrane and the other more proximally. The sensilla are arranged with their long axes roughly parallel to the circumference of the spigots. External forces, transmitted by the dragline, result in deformation of the central part of the cuticular plate at the base of the spigots and thus in stimulation of the sensilla. This is shown electrophysiologicallly. Considering their morphology, topography, and electrophysiology, these mechanoreceptors are suggested to be important in the sensory control of dragline release by the spider.     

Morphology and ontogeny of single-walled multiporous sensilla of hemimetabolous insects

Comparative morphological investigations were made to determine the common organization plan of single-walled multiporous sensilla. The development of multiporous chemoreceptive sensilla of Gryllus, Oncopeltus and Lepisma follows the same path. Each chemoreceptive sensillum is associated with four types of enveloping cell. During ontogeny, enveloping cell 1 secretes the dendritic sheath. Enveloping cell 4 builds the connection of the hair base with the antennal cuticle. In Gryllus and Oncopehus, enveloping cells 2 and 3 build the hair shaft, the wall pores and pore tubules in nearly equal parts. Enveloping cells 2 and 3 lie side by side in the hair process, in which enveloping cell 2 produces the inner part, enveloping cell 3 the outer part of the hair shaft. In Lepisma the predominant part of the hair shaft with the wall pores is formed by the doubled enveloping cells 3. Interpreting our findings and the literature data, a new proposal is given for the homology of the enveloping cells. In singlewalled chemoreceptors, enveloping cell 1 is considered as thecogen and enveloping cell 4 as tormogen cell. Enveloping cell 2 is interpreted as inner trichogcn cell and enveloping cell 3 as outer trichogen cell.     

The microfiber texture in a specialized plastic cuticle area within a sensillum field on the cockroach maxillary palp as revealed by freeze fracturing

A field of sensilla extends across the ventral surface of the terminal segment of the maxillary palps of Periplaneta americana. The sensilla project from a sheet of pliable cuticle. Ultrathin sections of the cuticle in this area reveal a clear-cut parabolic microfiber pattern. Microfibers can also be seen from freeze fracture faces running parallel to the cuticular surface. These microfibers have a diameter of 80 A and may consist of chitin crystallites surrounded by a matrix coat. The number of straight parallel microfibers visible in a fracture face increases the more closely parallel to the surface the fracture runs. This result suggests a helicoidal texture, as the model of Bouligand would demand. The layer-to-layer rotational displacement of the microfibers is about 12 degrees. This texture can be regarded as typical for flexible cuticles in general. Other structural properties such as the continuation of the epicuticular dense layer into deeper cuticular layers around the enveloping cells of sensilla can be interpreted as specializations connected with the function of the sensillum field.     

The morphology of spider sensilla. I. Mechanoreceptors

The common tactile hair sensilla of spider tarsi were studied in web spiders (Araneus) and ground spiders (Lycosa, Dugesiella) using scanning and transmission electron microscopy. All of these sensilla are innervated by three bipolar neurons whose dendrites end proximally at the sensillum base. Each dendritic terminal exhibits a tubular body, a dense array of microtubules typical for mechanoreceptive sensilla. A dendritic sheath encloses the outer dendritic segments and connects the dendritic terminals to cuticular components of the hair sensillum in three different ways: (1) A distal extension of the dendritic sheath connects to the midline of the hair base; (2) A forked arrangement of cuticular (?) strands attaches on both lateral sides of the hair base, and (3) The socket cuticle directly contacts a part of the dendritic sheath. The latter connection provides a fixed position for the three dendritic terminals and any movement of the hair shaft could be transmitted via connections (I) and (2). The triple innervation strongly suggests a directional sensitivity of these sensilla.Structural comparison between arachnid and insect mechanoreceptive sensilla indicates that tactile hair sensilla in Arachnida are multi-innervated whereas the corresponding reccptors in Insecta are singly innervated.     

The fine structure of campaniform sensilla on the halteres of Drosophila melanogaster

The campaniform sensilla on halteres of Drosophila were studied by electron microscopy in order to establish the relationships of functional elements in the sensory system. The surface of the sensillum consists of an oval cuticular cap membrane which may contain resilin, the rubberlike protein. A border of denser cuticle rings the cap membrane, and extending down around the neural process is a third type of cuticle filled with a fourth light fibrous type. The four cuticular components form a system for displacement of the neural process. The neural process is differentiated into a terminal fan-shaped structure projecting from a bulbous dilatation which tapers to a neck region ending proximally with two basal bodies. The neural process is packed with microtubules. Surrounding the dendrite is an inner enveloping cell, attached to the basal body region by septate desmosomes and by desmosomes to which microtubules of the enveloping cell are applied. An outer enveloping cell surrounds the inner one. The tip of the neural process is covered with a dense secretion which is tightly bound to the cap membrane. The dense secretion is surrounded by an extracellular fluid which might be compressed hydraulically by the cuticular system. The stimulus of cuticular distortion could thus be transmitted to the neural process which may be displaced between its fixed ends.     

The coelocapitular sensillum,an antennal hygro- and thermoreceptive sensillum of the honey bee,Apis mellifera L.

Summary The sensillum coelocapitulum, a hygro- and thermoreceptive sensillum of the honey bee, Apis mellifera, was investigated by electron microscopy. The cuticular apparatus of the sensillum is a mushroomshaped protrusion, devoid of pores, set in a narrow cylindrical pit positioned centrally within a cuticular, shallow depression. There may be three or four receptor cells. Three receptor cells have unbranched sensory cilia, containing densely packed microtubules, which extend distally into the cuticular apparatus and completely fill its cavity. These connecting cilia are of the usual 9+0 type. The fourth receptor, if present, has a thin sensory cilium which terminates beneath the cuticular apparatus. Its connecting cilium has armed outer doublets. The outer cavity is formed by two enveloping cells and is completely sealed off. Lipid deposits are present within the cavity and the tormogen cell. The thecogen cell has scolopale rod-like structures around the inner cavity. Features common to the insect hygro- and thermoreceptive sensilla are discussed in comparison with those of other insects.     

The cercal sensilla of the blowfly Lucilia cuprina. II. Structure of the enveloping cells and the basal regions of the sensory dendrites

The gustatory, olfactory, touch and stress receptors on the cerci of Lucilia cuprina Wied. (Diptera: Calliphoridae) have either two or three enveloping cells. The gustatory and olfactory sensilla have three enveloping cells: a tormogen, trichogen and thecogen cell. The tormogen and trichogen cells contribute to a sub-cuticular sensillar lumen which divides into two lobes basally. The thecogen cell forms a lumen around the dendrites. Distally the dendrites lie in the contents of the thecogen lumen within the dendritic sheath. Proximally the dendrites embed in the thecogen cell which has an expanded, microlamellate lumen basally. The sensillar lumen of the mechanosensory (trichoid mechanoreceptors and campaniform) sensilla is formed by a single enveloping cell: the presumptive tormogen cell. In trichoid mechanoreceptors the thecogen lumen is restricted to the region of the transitional region of the dendrite whereas the thecogen lumen of campaniform sensilla extends proximally although it is not as well-developed as that of the chemoreceptive sensilla. The dendrites of all sensillum types on the cerci have a granular body in the transitional region: a situation which has not been previously reported in chemoreceptive sensilla although common in the mechanoreceptors of Calliphoridae and Sarcophagidae.     

Sensory receptors on the adult labial and maxillary palpi and galea of Cicindela sexguttata (Coleoptera: Cicindelidae)

Five types of sensilla are situated on the apical area of the labial and maxillary palpi and galea of Cicidela sexguttata. Large, conical, and peg-like sensilla are in rows on the central region of each palpus. These sensilla have a hollow cuticular peg, with an apical pore and multi-innervation. This central region of palpal sensilla is surrounded by campaniform sensilla that are disc-shaped and small conical peg sensilla. A similar type of conical sensillum as the found in the palpal central region is situated around the periphery of the palpal apex and apex of the galea. This conical peg sensillum is located in a shallow depression and is structurally similar to the other peg sensilla, but it has a mechanoreceptor neuron attached to the cuticular base of the sensillum. A long, single, trichoid sensillum is situated in the center of the galea and is hollow, thick-walled, porous, and multi-innervated. The apices of the palpi and galea have a large number of dermal gland openings that actively secrete a substance during the feeding process of the tiger beetle. © 1995 Wiley-Liss, Inc.     

Ultrastructural studies of Haller's organ in the argasid tick, Argas tridentatus (Argasidae)]

Haller's organ in A. tridentatus consists of a capsule and an anterior group of sensilla. The capsule is the hollow in the cuticle on the dorsal surface of the first tarsus, where 4 pored hairs of olfactory sensilla are situated under the cover of the roof, formed by an anostomosis of the upper brunches of pleomorphs (capsule's bottom non-sensory cuticular outgrowths). The canal of the accessory ampullaceous sensillum opens in a capsule near the bottom. The anterior group of sensilla consists of two parts: proximal part, containing pored grooved and thin hairs, is homologous to the anterior grouf of ixodid ticks, and distal one which has no homologues in ixodids. Fine structure of all the sensilla in the mentioned parts of Haller's organ is described in detail.     

Are the most numerous sensilla of terrestrial isopods hygroreceptors? Ultrastructure of the dorsal tricorn sensilla of Porcellio scaber

The ultrastructure of the tricorn sensilla of the woodlouse Porcellio scaber was investigated in cryofixed and freeze-substituted, or chemically fixed specimens. The tricorn sensilla have a foramenized triangular-shaped outer hair and bear a poreless rod-like inner hair. The conical base of the inner hair is connected to the base of the outer hair by a complex cuticular structure. Each sensillum contains three sensory cells. The tip of one of the three dendrites contains a tubular body and is clamped between two bulges of the dendritic sheath. The two other dendrites protrude to the tip of the inner hair, flush against the cuticular wall. The microtubules in the ciliary segments are arranged in nine double tubuli that have neither osmiophilic cores nor arms. The ciliary rootlets are small. The inner segment of the largest dendrite wraps around the two smaller dendrites and one of seven enveloping cells in a mesaxon-like manner. Although this ultrastructure deviates considerably from most crustacean mechanosensitive sensilla, it nevertheless suggests a mechanosensitive function, at least for one of the sensory cells. In many aspects, the tricorn sensilla resemble the thermohygrosensilla of insects. However, our results suggest that the structural criteria for thermo-hygro-sensitivity used in insects cannot simply be applied to crustaceans.     

Die digitiformen Sensillen auf dem Maxillarpalpus von Coleoptera

Summary The digitiform sensilla on the distal segment of the maxillar palps ofAgabus bipustulatus (L.) andHydrobius fuscipes (L.) were investigated by electron microscopic methods. Each sensillum is innervated by a single bipolar sensory cell. The sensilla ofHydrobius are associated with three enveloping cells, which enclose an inner and outer receptor lymph cavity. A single enveloping cell only is found in the completely differentiated sensilla ofAgabus. These sensilla do not form an outer lymph cavity. The area beneath the hair base is filled by the distal process of the enveloping cell and by extensions of epidermal cells. Only one extra-cellular space exists, which seems to be homologous to an inner receptor lymph cavity.The outer dendritic segment surrounded by a dendritic sheath runs to the tip of the hair shaft. In the hair shaft the outer dendritic segment divides into several branches. The poreless hair shaft does not rise over the surface of the cuticle, but it is positioned in a narrow shallow groove. Special socket structures or a tubular body do not exist. The digiti-form sensilla possess neither the typical feature of mechanosensitive, nor gustatory or olfactory sensilla. The functional significance of the structural divergences in the sensilla of both species and the presumed function of the sensilla are discussed referring to hygro- and thermo-receptors.

Unserem verehrten Lehrer, Herrn Prof. Dr. H.Risler, dem wir für vielfache Förderung danken möchten, zum 65. Geburtstag gewidmet.     

Fine structure and role in behavior of sensilla on the terminalia of Aedes aegypti (L.) (Diptera: Culicidae)

The terminalia of male and female Aedes aegypti (L.) bear numerous hairs of various shapes and lengths, all of which are mechanoreceptors. Each hair is innervated by one bipolar neuron which contains ciliary rootlets, two basal bodies, and a region assuming the structure of a non-motile cilium. At the distal tip of the dendrite is a tubular body, a characteristic of cuticular mechanoreceptors. Covering the outer dendritic segment is a cuticular sheath which ends proximally in a net-like felt-work and distally attaches to the hair base. Each hair sensillum has two sheath cells. Presumed efferent fibers are associated with the sheath cells. On the insula of the female terminalia are a few campaniform sensilla, the domes of which are raised into small pegs. The sensilla on the terminalia function in copulation and oviposition and probably in warning. A sequence of neurological events is traced for copulation and oviposition. Other cuticular structures, viz., scales, microtrichia, acanthae, and aedeagal spines, which occur on the terminalia are not innervated.