Adhesive mechanisms in cephalopods: a review

Abstract

Several genera of cephalopods (Nautilus, Sepia, Euprymna and Idiosepius) produce adhesive secretions, which are used for attachment to the substratum, for mating and to capture prey. These adhesive structures are located in different parts of the body, viz. in the digital tentacles (Nautilus), in the ventral surface of the mantle and fourth arm pair (Sepia), in the dorsal epidermis (Euprymna), or in the dorsal mantle side and partly on the fins (Idiosepius). Adhesion in Sepia is induced by suction of dermal structures on the mantle, while for Nautilus, Euprymna and Idiosepius adhesion is probably achieved by chemical substances. Histochemical studies indicate that in Nautilus and Idiosepius secretory cells that appear to be involved in adhesion stain for carbohydrates and protein, whilst in Euprymna only carbohydrates are detectable. De-adhesion is either achieved by muscle contraction of the tentacles and mantle (Nautilus and Sepia) or by secretion of substances (Euprymna). The de-adhesive mechanism used by Idiosepius remains unknown.     

Old and sticky-adhesive mechanisms in the living fossil Nautilus pompilius (Mollusca, Cephalopoda)

Nautiloidea is the oldest group within the cephalopoda, and modern Nautilus differs much in its outer morphology from all other recent species; its external shell and pinhole camera eye are the most prominent distinguishing characters. A further unique feature of Nautilus within the cephalopods is the lack of suckers or hooks on the tentacles. Instead, the animals use adhesive structures present on the digital tentacles. Earlier studies focused on the general tentacle morphology and put little attention on the adhesive gland system. Our results show that the epithelial parts on the oral adhesive ridge contain three secretory cell types (columnar, goblet, and cell type 1) that differ in shape and granule size. In the non-adhesive aboral epithelium, two glandular cell types (cell types 2 and 3) are present; these were not mentioned in any earlier study and differ from the cells in the adhesive area. The secretory material of all glandular cell types consists mainly of neutral mucopolysaccharide units, whereas one cell type in the non-adhesive epithelium also reacts positive for acidic mucopolysaccharides. The present data indicate that the glue in Nautilus consists mainly of neutral mucopolysaccharides. The glue seems to be a viscous carbohydrate gel, as known from another cephalopod species. De-attachment is apparently effectuated mechanically, i.e., by muscle contraction of the adhesive ridges and tentacle retraction.     

Chamber growth in ammonites inferred from colour markings and naturally etched surfaces of Cretaceous vascoceratids from Nigeria

Cretaceous Vascoceras and Jurassic Lytoceras show colour markings and etched surfaces representing original organic membranes between the septa. The main difference between the formation of ammonite and Nautilus chambers involved the continuous secretion of a gelatinous cameral liquid to support the ammonite mantle when it moved forward. The gel containing cyclically secreted membranes. here named pseudosepta, resembled the intra-cameral structures of the cuttlebone in Sepia. Pseudoscpta are attached to the shell wall in pseudosutures (Pseudoloben) which are particularly visible in the saddles of the septal suture and tend to mimic them. Their shape suggests reconstruction of posterior mantle shape during translocation. Drag-bands (Schleppstreifen) are spiral markings formed by the overlapping pseudosepta along the axial traces of the foliole folds. The chamber of ammonites was formed by a locally muscular mantle in a tripartite cycle: (1) the mantle initially remained attached to the saddles of the completed septal suture while muscular tissue within the umbilical lobes was contracted and rapidly reattached to the side of the lateral saddles; (2) the whole mantle subsequently crept forward by secreting a gelatinous matrix which contained telescoped membranes, with an adhesive function on pseudolobc flanks; (3) the mantle almost ceased to move within the sites of future lobules, but expanded and crept on before forming the mural and 'gutter' ridges of the septum. □ Ammonites, chamber growth, vascoceratids, LYTOCERAS, Nigeria.     

Hatching glands in cephalopods – A comparative study

Hatching of embryos from their eggs involves either mechanical and/or chemical support. In particular enzymes are widely used in the animal kingdom to weaken the egg layers and facilitate the embryo's escape. Although numerous morphological and biochemical studies exist on the hatching glands of invertebrates (such as sea urchins, ascidians, insects) and vertebrates (teleosts, amphibians, and mammals), little is known about the morphology of the hatching glands (Hoyle organs) in cephalopod hatchlings.In this study, the internal gland structure and the external appearance of the Hoyle organ are compared among several cephalopod species (Idiosepius pygmaeus; Euprymna scolopes; Sepia officinalis; Loligo gahi; Sepioteuthis lessoniana; Architeuthis sp.; Octopus vulgaris; Tremoctopus gracilis; Argonauta hians). In almost all cases the glandular system is restricted to the posterior part of the dorsal mantle surface. Only Octopus and Argonauta lack a specific glandular structure in this body region and the animals apparently use other mechanisms to penetrate the egg layers.In all decapod species (Idiosepius; Euprymna; Sepia; Loligo; Sepioteuthis; Architeuthis) as well as in Tremoctopus only one specific cell type is present in the Hoyle organ, which synthesizes granular material. The secretory droplets are more or less uniform in electron density in Idiosepius, Euprymna and Tremoctopus but exhibit translucent inclusions in the other decapods. The time of gland development, first synthesis of secretory products and later degeneration after hatching vary between the species.The present study contributes to our knowledge of glandular systems in cephalopods and allows comparison with hatching structures in other invertebrates and vertebrates.     

Evolution of the cephalopod head complex by assembly of multiple molluscan body parts: Evidence from Nautilus embryonic development

Cephalopod head parts are among the most complex occurring in all invertebrates. Hypotheses for the evolutionary process require a drastic body-plan transition in relation to the life-style changes from benthos to active nekton. Determining these transitions, however, has been elusive because of scarcity of fossil records of soft tissues and lack of some of the early developmental stages of the basal species. Here we report the first embryological evidence in the nautiloid cephalopod Nautilus pompilius for the morphological development of the head complex by a unique assembly of multiple archetypical molluscan body parts. Using a specialized aquarium system, we successfully obtained a series of developmental stages that enabled us to test previous controversial scenarios. Our results demonstrate that the embryonic organs exhibit body plans that are primarily bilateral and antero-posteriorly elongated at stereotyped positions. The distinct cephalic compartment, foot, brain cords, mantle, and shell resemble the body plans of monoplacophorans and basal gastropods. The numerous digital tentacles of Nautilus develop from simple serial and spatially-patterned bud-like anlagen along the anterior-posterior axis, indicating that origins of digital tentacles or arms of all other cephalopods develop not from the head but from the foot. In middle and late embryos, the primary body plans largely change to those of juveniles or adults, and finally form a "head" complex assembled by anlagen of the foot, cephalic hood, collar, hyponome (funnel), and the foot-derived epidermal covers. We suggest that extensions of the collar-funnel compartment and free epidermal folds derived from multiple topological foot regions may play an important role in forming the head complex, which is thought to be an important feature during the body plan transition.     

The ultrastructure of the tentacles of eleven species of dendrochirote holothurians studied with special reference to the surface coats and papillae

Summary The tentacles of eleven species of dendrochirote holothurians have been studied. The water vascular system, deep fibre system, ectoneural nerve ring and superficial fibre system are described and are similar to those of other holothurian tentacles. A conspicuous fuzzy coat covers the entire tentacular surface except for the tips of cilia. On the basis of its structure it is thought to be an attenuated glycocalyx. Its function is discussed in relation to anti-fouling and surface adhesion. The two surface coats underlying the fuzzy coat are termed the cuticle. Bacteria are found both within the surface coats and in the sub-cuticular space. Primary fixatives lacking osmium give poor preservation of the surface coats. The adhesive papillae of the apices of the tentacles contain elements of support cells and two other cells named Type-1 and Type-2 papillar cells. The secretions of Type-1 papillar cells are dense-cored vesicles and may contain a proteinaceous adhesive. The vesicles fuse with the cuticle and release their products which are apparently disseminated along the fuzzy coat filaments. The secretions of Type-2 papillar cells may have a neurosecretory function. The different models of food capture by dendrochirote tentacles are discussed as are duo-glandular adhesive systems in relation to dendrochirote tentacles.     

Pax6 in the sepiolid squid Euprymna scolopes: evidence for a role in eye,sensory organ and brain development

The cloning of a Pax6 orthologue from the sepiolid squid Euprymna scolopes and its developmental expression pattern are described. The data are consistent with the presence of a single gene encoding a protein with highly conserved DNA-binding paired and homeodomains. A detailed expression analysis by in situ hybridization and immunodetection revealed Pax6 mRNA and protein with predominantly nuclear localization in the developing eye, olfactory organ, brain lobes (optic lobe, olfactory lobe, peduncle lobe, superior frontal lobe and dorsal basal lobe), arms and mantle, suggestive of a role in eye, brain, and sensory organ development.     

Renal organs of cephalopods: a habitat for dicyemids and chromidinids

The renal organs of 32 species of cephalopods (renal appendage of all cephalopods, and renal and pancreatic appendages in decapods) were examined for parasite fauna and for histological comparison. Two phylogenetically distant organisms, dicyemid mesozoans and chromidinid ciliates, were found in 20 cephalopod species. Most benthic cephalopods (octopus and cuttlefish) were infected with dicyemids. Two pelagic cephalopod species, Sepioteuthis lessoniana and Todarodes pacificus, also harbored dicyemids. Chromidinid ciliates were found only in decapods (squid and cuttlefish). One dicyemid species was found in branchial heart appendages of Rossia pacifica. Dicyemids and chromidinids occasionally occurred simultaneously in Euprymna morsei, Sepia kobiensis, S. peterseni, and T. pacificus. The small-sized cephalopod species, Idiosepius paradoxus and Octopus parvus, harbored no parasites. Comparative histology revealed that the external surface of renal organs varies morphologically in various cephalopod species. The small-sized cephalopod species have a simple external surface. In contrast, the medium- to large-sized cephalopod species have a complex external surface. In the medium- to large-sized cephalopod species, their juveniles have a simple external surface of the renal organs. The external surface subsequently becomes complicated as they grow. Dicyemids and chromidinids attach their heads to epithelia or insert their heads into folds of renal appendages, pancreatic appendages, and branchial heart appendages. The rugged and convoluted external surface provides a foothold for dicyemids and chromidinids with a conical head. They apparently do not harm these tissues of their host cephalopods.     

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.     

7种头足类动物墨汁的钠、钾含量分析

采用火焰光度计测定法,对虎斑乌贼(Sepia pharaonis)、金乌贼(Sepia esculenta)、拟目乌贼(Sepial ycidas)、日本无针乌贼(Sepiella japonica)、柏氏四盘耳乌贼(Euprymna berryi)(乌贼目)、剑尖枪乌贼(Uroteuthis edulis)(枪形目)和弯斑蛸(Octopus dollfusi)(八腕目)等7种头足类动物墨汁中的钠、钾含量进行了检测.结果显示:乌贼目墨汁的钠含量比八腕目和枪形目高.五种乌贼目动物中,金乌贼与拟目乌贼、日本无针乌贼、柏氏四盘耳乌贼,拟目乌贼与虎斑乌贼,虎斑乌贼与日本无针乌贼的墨汁钠含量存在显著的差异(P＜0.05),其余的组合无显著差异.不同目的动物墨汁的钾含量无明显的差异.     

Morphological and behavioral evidence for adaptive diversification of sympatric Hawaiian limpets (Cellana spp.)

The endemic Hawaiian limpets (Cellana exarata, Cellana sandwicensis, and Cellana talcosa), reside at different elevations on wave-exposed rocky shores and comprise a monophyletic lineage that diversified within Hawai'i. Here, I report phenotypic differences in shell, soft tissue, and behavioral characters among these limpets and discuss their potential utility in exploiting their respective niches. The high-shore limpet, C. exarata, is characterized by a tall round shell, short mantle tentacles, and long evasion distance when confronted by a predatory gastropod. The mid-shore limpet, C. sandwicensis, is characterized by a shorter oblong shell, long mantle tentacles, and a short evasion distance when confronted by a predatory snail. The low-shore, shallow-subtidal limpet, C. talcosa, is characterized by a flat shell that is thin in juveniles and disproportionately massive in large adults (relative to the other two species), and mantle tentacles of varying lengths (some individuals exhibit short tentacles, some long). These species-specific suites of characters are likely to confer specific fitness advantages on the high shore (C. exarata) where thermal and desiccation stress is severe, on the mid shore (C. sandwicensis) where hydrodynamic forces are severe, and on the low-shallow subtidal shore (C. talcosa) where pelagic predators have free access to the limpets. These data add to the growing body of evidence for adaptive diversification and speciation in the Hawaiian Cellana, and in marine species in general.     

Hemocyanin and the branchial heart complex of Sepia officinalis: are the hemocytes involved in hemocyanin metabolism of coleoid cephalopods?

Cytobiological experiments using isotopic- and cytochemical-labeled Sepia hemocyanin as well as immunocytochemical localization of the respiratory pigment were carried out to investigate the function of the hemocytes in hemocyanin metabolism of the common cuttlefish Sepia officinalis. For comparison, the rhogocytes (ovoid cells) of the branchial heart complex were included in this study. Hemocyanin molecules were immunocytochemically detected in the lysosomal compartment of the rhogocytes and, at lower levels, in adhesive and circulating hemocytes. (125)I-labeled Sepia hemocyanin was taken up by the rhogocytes only, whereas gold- and/or fluorescein-labeled Sepia hemocyanin was solely taken up by the adhesive and the circulating hemocytes, even though the level of uptake is different. There are also differences in the uptake of pure gold particles and/or fluorescein between rhogocytes and hemocytes. These findings give evidence that circulating and adhesive hemocytes of the branchial heart complex are not involved in hemocyanin turnover, but are a component of the cellular defense and detoxification system of adult coleoid cephalopods.     

Structure of the brachiopod lophophore

Data on the development, structure, and functional morphology of the brachiopod lophophore are analyzed. The common origin of the tentacle apparatus in Lophophorata from the postoral ciliary band of the larva is shown. The brachiopod lophophore is based on the brachial axis consisting of the brachial fold running along the row of tentacles. The brachial axis may be attached to the brachial (dorsal) mantle lobe (trocholophe, schizolophe, and ptycholophe lophophores) or extend freely into the mantle cavity to form coiling brachia (spirolophe, zygolophe, and plectolophe lophophores). The circulation of water flows through the mantle cavity in the brachiopods with attached and free lophophores is described. A new hypothesis on the sorting of particles suspended in water during filtration is proposed.     

Morphological,ultrastructural and histochemical investigation of epipodial sensory structures of Haliotis tuberculata (Gastropoda: Haliotidae)

In this study, we describe the microstructure and ultrastructure of the epipodial papillae and epipodial tentacles of Haliotis tuberculata using light and electron microscopy. The epipodial papillae vary morphologically; they are subdivided into several subpapillae whose surface is covered by small micropapillae. The epipodial tentacles are large extendable conically elongated structures whose surface is differentiated in two regions: the dorsal region with long corrugated folds, and a ventral region composed of three parts, a basal part with the same structure as the dorsal, a middle part with shorter corrugated folds and an apical part with large micropapillae. Although the thin sections and ultrastructure examination show that the epithelium of both organs is morphologically similar and composed of supporting cells, sensory cells and different types of secretory cells, there is a certain specialization in their secretory product. Although the epithelium of both structures was positive for acidic glycoconjugates, the tentacle epithelium was also positive for neutral sugars. Further specific differences were revealed by lectin histochemistry. Because papillae and tentacles can be extended or retracted depending on environmental conditions, they probably have tactile and olfactory functions.     

Differentiation of slow and fast fibers in tentacles of Sepia officinalis (Mollusca)

The tentacles of Sepia officinalis are cylindrical muscular structures that can be quickly everted and elongated to capture prey. The combination of both velocity and extensive elongation of the tentacles is due to the presence of both cross-striated and helical muscles. The complex organization and differentiation of different fibers has been studied in cuttlefish extracted from egg gel coats at different developmental stages, and in completely developed animals. Tentacle muscles start to differentiate centrifugally from the area close to the axial nervous system, where two types of myocytes can be recognized. These populations of myocytes, which may be distinguished morphologically and which express different myosin isoforms, give rise to fast and slow muscles. The presence in molluscs of slow and fast muscles arising from different populations of myocytes, as in vertebrate muscle development, could be considered as an example of evolutionary conservation.     

Components of the cellular defense and detoxification system of the common cuttlefish Sepia officinalis (Mollusca,Cephalopoda)

Endocytotic-active cells in the branchial heart complex of Sepia officinalis were studied by in situ injection of different types of xenobiotics and by in vitro perfusion of the organ complex with a bacterial suspension. The rhogocytes (ovoid cells) ingest particles of all tested sizes by endocytosis and phagocytosis. The hemocytes of the circulating blood and the adhesive hemocytes in the wall of the branchial heart incorporate all tested kinds of foreign materials, including bacterial cells due to phagocytosis achieved by the triangular mesenchymatic cells. The ultrastructural findings also give strong evidence that the triangular mesenchymatic cells are fixed hemocytes that have migrated into the branchial heart tissue. The ingestion and digestion of allogeneic substances and bacteria or their debris by rhogocytes and/or all (forms of) hemocytes suggests the involvement of these either fixed or mobile endocytotic-active cells in the defense and detoxification system of cephalopods.