Wiring a periscope--ocelli, retinula axons, visual neuropils and the ancestrality of sea spiders

The Pycnogonida or sea spiders are cryptic, eight-legged arthropods with four median ocelli in a ‘periscope’ or eye tubercle. In older attempts at reconstructing phylogeny they were Arthropoda incertae sedis, but recent molecular trees placed them as the sister group either to all other euchelicerates or even to all euarthropods. Thus, pycnogonids are among the oldest extant arthropods and hold a key position for the understanding of arthropod evolution. This has stimulated studies of new sets of characters conductive to cladistic analyses, e.g. of the chelifores and of the hox gene expression pattern. In contrast knowledge of the architecture of the visual system is cursory. A few studies have analysed the ocelli and the uncommon “pseudoinverted” retinula cells. Moreover, analyses of visual neuropils are still at the stage of Hanström''s early comprehensive works. We have therefore used various techniques to analyse the visual fibre pathways and the structure of their interrelated neuropils in several species. We found that pycnogonid ocelli are innervated to first and second visual neuropils in close vicinity to an unpaired midline neuropil, i.e. possibly the arcuate body, in a way very similar to ancestral euarthropods like Euperipatoides rowelli (Onychophora) and Limulus polyphemus (Xiphosura). This supports the ancestrality of pycnogonids and sheds light on what eyes in the pycnogonid ground plan might have ‘looked’ like. Recently it was suggested that arthropod eyes originated from simple ocelli similar to larval eyes. Hence, pycnogonid eyes would be one of the early offshoots among the wealth of more sophisticated arthropod eyes.     

Pigmented eyes,photoreceptor‐like sense organs and central nervous system in the polychaete Scoloplos armiger (Orbiniidae,Annelida) and their phylogenetic importance

The phylogenetic position of Orbiniidae within Annelida is unresolved. Conflicting hypotheses place them either in a basal taxon Scolecida, close to Spionida, or in a basal position in Aciculata. Because Aciculata have a specific type of eye, the photoreceptive organs in the orbiniid Scoloplos armiger were investigated to test these phylogenetic hypotheses. Two different types of prostomial photoreceptor‐like sense organs were found in juveniles and one additional in subadults. In juveniles there are four ciliary photoreceptor‐like phaosomes with unbranched cilia and two pigmented eyes. The paired pigmented eyes lie beside the brain above the circumoesophageal connectives. Each consists of one pigmented cell, one unpigmented supportive cell and three everse rhabdomeric sensory cells with vestigial cilia. During development the number of phaosomes increases considerably and numerous unpigmented sense organs appear consisting of one rhabdomeric photoreceptor cell and one supportive cell. The development and morphology of the pigmented eyes of S. armiger suggest that they represent miniaturized eyes of the phyllodocidan type of adult eye rather than persisting larval eyes resulting in small inverse eyes typical of Scolecida. Moreover, the structure of the brain indicates a loss of the palps. Hence, a closer relationship of Orbiniidae to Phyllodocida is indicated. Due to a still extensive lack of ultrastructural data among polychaetes this conclusion cannot be corroborated by considering the structure of the unpigmented ciliary and rhabdomeric photoreceptor‐like sense organs. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Zur Ultrastruktur der seitlichen Sinnesorgane am Augenhügel vonAnoplodactylus pygmaeus (Pycnogonida)

Former light microscopic studies on the lateral sense organs of sea spiders yielded divergent results. Consequently, different authors ascribed different functions to these organs. The present ultrastructural study shows that each lateral sense organ ofA. pygmaeus consists of approximately 15 sensory cells of two different types, approximately 20 sheath cells with numerous long microvilli, and an outer cuticular covering. Essentially the same elements are characteristic features of arthropod sensilla. There are, however, differences between the sense organs described in this paper and the sense organs of other arthropods. The inner dendritic segments of sensory cells S₁ of theA. pygmaeus lateral sense organs are very short, the sensory cilia are invaginated, and the pericarya of the sensory cells contain electron lucent cytoplasmic regions with large granules (glycogen?). In addition, the lateral sense organs ofA. pygmaeus lack a marked receptor lymph cavity and junctions between the cells. The results of the present ultrastructural study clearly indicate that the lateral sense organs ofA. pygmaeus are not glands as was postulated for other sea spider species by earlier authors. Some investigators hypothesized that the lateral sense organs of other sea spider species were auditory organs or rudimentary eyes. The present results do not support such speculations. Some structural details of the sensory cells ofA. pygmaeus resemble those found in chemoreceptive or putative chemoreceptive organs of other arthropods. Accordingly, chemoreceptive or thermoreceptive functions should be taken into consideration for the lateral sense organs ofA. pygmaeus.     

Comments on the eyes of tardigrades

A survey is given on the scarce information on the visual organs (eyes or ocelli) of Tardigrada. Many Eutardigrada and some Arthrotardigrada, namely the Echiniscidae, possess inverse pigment-cup ocelli, which are located in the outer lobe of the brain, and probably are of cerebral origin. Occurrence of such organs in tardigrades, suggested as being eyeless, has never been checked. Depending on the species, response to light (photokinesis) is negative, positive or indifferent, and may change during the ontogeny. The tardigrade eyes of the two eutardigrades examined up to now comprise a single pigment cup cell, one or two microvillous (rhabdomeric) sensory cells and ciliary sensory cell(s). In the eyes of the eutardigrade Milnesium tardigradum the cilia are differentiated in an outer branching segment and an inner (dendritic) segment. Because of the scarcity of information on the tardigrade eyes, their homology with the visual organs of other bilaterians is currently difficult to establish and further comparative studies are needed. Thus, the significance of these eyes for the evolution of arthropod visual systems is unclear yet.     

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.     

Sense organs in polychaetes (Annelida)

Polychaetes possess a wide range of sensory structures. These form sense organs of several kinds, including the appendages of the head region (palps, antennae, tentacular cirri), the appendages of the trunk region and pygidium (parapodial and pygidial cirri), the nuchal organs, the dorsal organs, the lateral organs, the eyes, the photoreceptor-like sense organs, the statocysts, various kinds of pharyngeal papillae as well as structurally peculiar sensory organs of still unknown function and the apical organs of trochophore larvae. Moreover, isolated or clustered sensory cells not obviously associated with other cell types are distributed all over the body. Whereas nuchal organs are typical for polychaetes and are lacking only in a few species, all other kinds of sensory organs are restricted to certain groups of taxa or species. Some have only been described in single species till now. Sensory cells are generally bipolar sensory cells and their cell bodies are either located peripherally within the epidermis or within the central nervous system. These sensory cells are usually ciliated and different types can be disinguished. Structure, function and phylogenetic importance of the sensory structures observed in polychaetes so far are reviewed. For evaluation of the relationships of the higher taxa in Annelida palps, nuchal organs and pigmented ocelli appear to be of special importance.     

Fine Structure of the ‘Slit Organs’ of the Pycnogonid Anoplodactylus petiolatus (Anoplodactylidae)

Abstract The ‘slit organs’ of Anoplodactylus petiolatus are found all over the body cuticle. They are composed of a cuticular pore apparatus, an inner and an outer canal cell, and of four large and one to three small compartment cells. Plasma of the latter seven cells is almost completely filled with large membrane-enclosed compartments that contain either numerous small vesicles (one of the large cells) or homogeneous material of varying electron density (three large and all the small cells). Microvilli are found in the apical region of the compartment cells. The nucleus is situated basally where Golgi-cisternae, coated vesicles and free ribosomes are frequently found. Apical microvilli and vesicles are also formed by the inner canal cell indicating that it might directly be involved in transport. Anatomically the ‘slit organs’ are similar to class III glands described for many arthropods. In addition, discharge of secretion via large intracellular compartments is also a feature found in arthropod glands. Although pycnogonids appear to take up substances across the cuticle, a genuine secretion rather than a more generalized transport function is suggested for the ‘slit organs’.     

Ultrastructural investigations on the nuchal organ of the protandric polychaete,Ophryotrocha puerilis (Polychaeta,Dorvilleidae)

Summary The nuchal organs of the protandric hermaphrodite Ophryotrocha puerilis were studied by electron microscopy. Ophryotrocha puerilis is the first species hitherto described which possesses four instead of two nuchal organs. These sensory structures are located as ciliary pits at the posterior margin of the prostomium. Histologically, the nuchal organs are composed of supporting cells with long motile cilia and bipolar sensory cells, the perikarya of which form four distinct nuchal ganglia adjoining the brain. These structural components are concentrically arranged around the central sensory area. This area is covered by a modified cuticle, whereas the cuticle above the peripheral region of the sense organ exhibits the appearance typical for polychaetes. Two types of vesicular material are produced in the basal supporting cells, a dense-cored one within the central supporting cells only and a clear irregular-shaped one in all of these cells. The first type is considered to be responsible for the formation of the modified cuticle. The significance of these most probably long-distance chemoreceptory organs and their possible role in reproductive behaviour is discussed.     

The Heart Ultrastructure in Two Species of Pycnogonids, and its Phylogenetic Implications

The heart of the pycnogonids Nymphon (Chaetonymphon) macronyx G. O. Sars and Boreonymphon cf. abyssorum Norman is pseudotubular and lacks an epicardium and an endocardium. The body wall forms the roof over the heart lumen. The myocardium is innvervated, and forms the lateral walls of the heart. Myofibres are absent in the midventral floor. This part is formed by cells of the horizontal septum attached to the gut complex. The myofibres are short. Interdigitating intercalated discs have not been observed, but lateral overlaps are common. Z-, I- and A-bands are seen in the sarcomere. The 2-bands are diffuse and irregular. The sarcolemma invaginates and forms a sparse system of clefts; a poorly developed T-system is indicated. Its presence supports the view that a T-system is inherent in the arthropod myocardium. Couplings are not related to any specific sarcomere band level. It is implied that the thin-walled pseudotubular heart in pycnogonids is a result of a reduction, and that it functions more like a channel than a heart.     

Fine structure and ecdysis of mandibular sensilla associated with the lacinia mobilis in Neomysis integer (Leach, 1814) (Crustacea,Malacostraca, Peracarida)

The external and internal structures of adult Neomysis integer mandibles were studied using light and electron microscopy with special reference to the lacinia mobilis, a highly specialized appendage on the gnathal edge of many crustaceans. The right and left lacinia mobilis are equipped with ciliary primary sensory cells revealing that both laciniae are also mechanosensory organs in addition to their mechanical function during mastication. A detailed character analyses indicated that the right lacinia is probably a highly derived sensory seta, whereas two alternative interpretations are considered for the left lacinia; it could be a sensillar appendage equipped with two mechanosensory units, or it could be a movable appendage of the incisor process containing two sensilla deprived of external appendages. The ecdysis of the lacinia mobilis corresponds very well to type I sensillar ecdysis, suggesting classification as a sensillar appendage. These features support a possible homology of the right lacinia mobilis in Peracarida and Decapoda, tracing them to an origin as a member of the setal row. Whether the left lacinia mobilis is a sensillum or an appendage with sensilla cannot be resolved presently.     

New sea spiders from the Jurassic La Voulte-sur-Rhône Lagerstätte

The diverse and exceptionally well-preserved pycnogonids described herein from the Middle Jurassic La Voulte Lagerstätte fill a 400 Myr gap of knowledge in the evolutionary history of this enigmatic group of marine arthropods. They reveal very close morphological and functional (locomotion, feeding) similarities with present-day pycnogonids and, by contrast, marked differences with all Palaeozoic representatives of the group. This suggests a relatively recent, possibly Mesozoic origin for at least three major extant lineages of pycnogonids (Ammotheidae, Colossendeidae, Endeidae). Combined evidence from depositional environment, faunal associates and recent analogues indicate that the La Voulte pycnogonids probably lived in the upper bathyal zone (ca 200 m). Our results point to a remarkable morphological and ecological stability of this arthropod group over at least 160 Myr and suggest that the colonization of the deep sea by pycnogonids occurred before the Jurassic.     

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.     

Fine structure of the galeal styloconic sensilla of larval Lymantria dispar (Lepidoptera: Lymantriidae)

Lepidopteran larvae possess two pairs of styloconic sensilla located on the maxillary galea. These sensilla, namely the lateral and medial styloconic sensilla, are each comprised of a smaller cone, which is inserted into a style. They are thought to play an important role in host-plant selection and are the main organs involved in feeding. Ultrastructural examination of these sensilla of fifth instar Lymantria dispar (L.) larvae reveal that they are each approximately 70 um in length and 30 um in width. Each sensillum consists of a single sensory peg inserted into the socket of a large style. Each peg bears a slightly subapical terminal pore averaging 317 nm in lateral and 179 nm in medial sensilla. Each sensillum houses five bipolar neurons. The proximal dendritic segment of each neuron gives rise to an unbranched distal dendritic segment. Four of these dendrites terminate near the tip of the sensillum below the pore and bear ultrastructural features consistent with contact chemosensilla. The fifth distal dendrite terminates near the base of the peg and bears ultrastructural features consistent with mechanosensilla. Thus, these sensilla each bear a bimodal chemo-mechanosensory function. The distal dendrites lie within the dendritic channel and are enclosed by a dendritic sheath. The intermediate and outer sheath cells enclose a large sensillar sinus, whereas the smaller ciliary sinus is enclosed by the inner cell. The neurons are ensheathed successively by the inner, intermediate, and outer sheath cells.     

Photoreceptor cells and eyes in Annelida

The evolution of photoreceptor cells and eyes in Metazoa is far from being resolved, although recent developmental and morphological studies provided strong evidence for a common origin of photoreceptor cells and existence of sister cell types in early metazoans. Photoreceptor cells are of two types, rhabdomeric and ciliary, depending on which part of the cells is involved in photoreception proper. A crucial point in understanding eye evolution is the explanation of the enormous structural diversity of photoreceptor cells and visual systems, given the general tendency for molecular conservation. One example of such diversity occurs in Annelida. In this taxon three types of photoreceptor cells exist: rhabdomeric, ciliary and phaosomous sensory cells. Whether the latter evolved independently or have been derived from one of the former cell types is still unresolved, since cilia and microvilli are found in these cells. These different photoreceptor cells are present in cerebral ocelli and eyes, in various ectopic ocelli and eyes situated in different places as well as in various photoreceptor-like sense organs. Whereas rhabdomeric cells mostly occur in connection with pigmented supportive cells, the other types are usually found with unpigmented supportive cells. Thus for the latter cells clear evidence for photoreception is still lacking in most cases. However, initial molecular-developmental investigations have shown that in fact ciliary photoreceptor cells exist within Annelida. Certain visual systems are only present during the larval phase and either replaced by the adult eyes or completely reduced during postlarval and adult stages. In the present paper the diversity of cerebral and extracerebral photoreceptor cells and ocelli as well as corresponding organs devoid of shading pigment is reviewed in Annelida.     

Sense Organs of Two Marine Arthrotardigrades (Heterotardigrada,Tardigrada)

The sense organs of the marine arthrotardigrades Halechiniscus greveni Renaud-Mornant & Deroux and Batillipes noerrevangi Kristensen were investigated with the aid of interference phase-contrast and transmission electron microscopy. The sense organs of the two species are quite different in outer cuticular morphology, but the inner cellular parts are constructed after the same model: the arthropod sensory setae. All investigated sensilla contained ciliary structures. Regeneration of the cirri during moult is very similar to the regeneration process in insects and spiders, but in the two arthrotardigrades the trichogen cell is not retracted from the cuticular part of the setae after moult. The clava is presumed to be olfactory; the cephalic cirri and the leg spines are contact chemoreceptors with one mechanoreceptive cilium terminating at the sensillum shaft. Cirrus E is compared with the trichobothrium of arthropods and the phylogenetic implications of the investigated structures are discussed.     

Arthropod Cladistics: Combined Analysis of Histone H3 and U2 snRNA Sequences and Morphology

Morphological, developmental, ultrastructural, and gene order characters are catalogued for the same set of arthropod terminals as we have scored in a recent study of histone H3 and U2 snRNA sequences (D. J. Colgan et al. , 1998, Aust. J. Zool. 46, 419–437). We examine the implications of separate and simultaneous analyses of sequence and non-sequence data for arthropod relationships. The most parsimonious trees based on 211 non-sequence characters (273 apomorphic states) support traditional higher taxa as clades, including Mandibulata, Crustacea, Atelocerata, Myriapoda, and Hexapoda. Combined analysis of morphology with histone H3 and U2 sequences with equal character weights differs from the morphological results alone in supporting Progoneata + Hexapoda (= Labiophora) in favor of a monophyletic Myriapoda, resolves the entognathous hexapods as a grade, and supports pycnogonids as sister group to Euchelicerata (rather than as basal euarthropods). Monophyly of Chelicerata (including pycnogonids), Mandibulata, Crustacea, Progoneata, Chilopoda, and Hexapoda is maintained under a range of transition/transversion and third codon weights, whereas Atelocerata and Myriapoda/Labiophora do not withstand all sensitivity analyses.     

Atlas of olfactory organs of Drosophila melanogaster 2. Internal organization and cellular architecture of olfactory sensilla

Antennae and maxillary palps of Drosophila melanogaster were studied with the electron microscope on serial sections of cryofixed specimens. The number of epidermal cells roughly equals the number of sensilla, except for regions where the latter are scarce or absent. Each epidermal cell forms about two non-innervated spinules, a prominent subcuticular space and a conspicuous basal labyrinth, suggesting a high rate of fluid transport through the sensory epithelium. The internal organization and fine structure of trichoid, intermediate and basiconic sensilla is very similar. Receptor cell somata are invested by thin glial sheaths extending distad to the inner dendritic segments. Further distally, the thecogen cell forms a sleeve around the dendrites, but an extracellular dendrite sheath is absent. At the base of the cuticular apparatus, the inner sensillum-lymph space around the ciliary and outer dendritic segments is confluent with the large outer sensillum-lymph space formed by the trichogen and tormogen cells. All three auxiliary cells exhibit many features of secretory and transport cells but extend only thin basal processes towards the haemolymph sinus. The bauplan and fine structure of coeloconic sensilla differs in the following aspects: (1) the ciliary segment of the dendrites is located deeper below the base of the cuticular apparatus than in the other sensillum types; (2) a prominent dendrite sheath is always present, separating inner and outer sensillum-lymph spaces completely; (3) the apical microlamellae of the auxiliary cells are more elaborate, but free sensillum-lymph spaces are almost absent; (4) there are always four not three auxiliary cells. Morphometric data are presented on the diameter of inner and outer dendritic segments and on the size of receptor cells, as well as of the receptor and auxiliary cell nuclei. The special fine structural features of Drosophila olfactory sensilla are discussed under the aspects of sensillar function and the localization of proteins relevant for stimulus transduction.     

The presence of statocysts and statoliths in social wasps (Hymenoptera, Vespinae)

Static sense organs composed of a hollow statocyst surrounded by sensory hairs and containing aggregate bodies (statoliths) have been detected in various species of Vespinae. On the frons in the groove traversing its center (the frontal groove) there is a deep pit and around it a membrane enclosing a cyst-like sac. In Vespa orientalis there are silicon (Si) and calcium (Ca)-containing aggregates inside the pit arranged in morula-like fashion, and in V. crabro, there are similar aggregates arranged in an ear-like shape. In general this sensillar organ resembles the statocyst located on the bases of the antennules in decapod crustaceans.     

New sense organ in larval hookworms.

A new ciliary sense organ is described which is bilaterally arranged, one in each lateral cord. It is just posterior to the nerve ring and adjacent to the excretory duct. The cilium is closely associated with another structure which is itself connected to the cuticle beneath the lateral alae. A nervous circuit is proposed which links this receptor via the hemizonid to the nerve ring. The receptor and associated structures are in the infective larvae of Necator americanus and Ancylostoma tubaeforme.