Endoscopy of gastropods: A novel view of the mantle cavities and gills of the keyhole limpet Diodora aspera and the abalone Haliotis rufescens

The gills, or ctenidia, of marine gastropods serve as the sites for respiratory gas exchange. Cilia on the surface provide the pump that moves water through the mantle cavity and enhance diffusion. Because the gills are housed inside the shell, it is difficult to view them while they are functioning. Published images of gills show contracted, fragile structures that are distorted by the processes of dissection and preservation. Members of the families Fissurellidae (keyhole limpets) and Haliotidae (abalone) have openings in their shells through which water enters and/or exits. I inserted an endoscope connected to a video camera into the openings of the shells of living, non‐anaesthetized individuals of the fissurellid Diodora aspera and the haliotid Haliotis rufescens. In both species, the dorsal afferent branchial vessel of the afferent gill axis appeared large and inflated, as did the leaflets that extended from either side of the axis. In D. aspera, the leaflets appeared to fill the mantle cavity and responded to touch, particles, and dye in the water by contracting quickly and slowly re‐extending. In contrast, the gills of H. rufescens did not noticeably respond to disturbance. On the other hand, these gills showed a regular pattern of pleats that had not been described in the extensive anatomical literature of these common and economically significant animals. These results provide a novel view of the gastropod mantle cavity as a dynamic space filled by the gills, which divide the mantle cavity into distinct incurrent and excurrent chambers and produce a laminar flow of water through the cavity. J. Morphol. 276:787–796, 2015. © 2015 Wiley Periodicals, Inc.     

The colour patterns of cypraeid gastropods

Colour patterns on mollusc shells are usually controlled by one-dimensional morphogenetic programmes. In adult cypraeids, by comparison, colour patterns are two-dimensional in morphogenesis and three-dimensional in structure. Visible patterns usually result from the uneven thickness of a pigmented layer, rather than from a spatially uneven concentration of pigment. Specialized sculptures in a few cypraeids may be regarded as extreme examples of three-dimensional colour patterns. Morphogenesis of some patterns is controlled by three-dimensional relief of the underlying shell surface. Computer models successfully reproduce key characteristics of cypraeid colour patterns. Since most cypraeids possess colour patterns, while few of the combinations of factors controlling these programmes yield a pattern, these patterns can be expected to have a yet undemonstrated adaptive value.     

Inherited abnormal growths on the mantle of Biomphalaria glabrata

Studies involved tissue growths in four different abnormal locations associated with the mantle of Biomphalaria glabrata: on the medial surface of the pseudobranch, projecting from the end of the dorsal ridge, inside the aperture on the right side, and at the base of the rectal fold in the ventral mantle chamber. Each type of growth was observed in only one or a few stocks of B. glabrata. Laboratory observations through several generations, with selection and reproduction of isolated snails by self-fertilization, suggested the tendency for formation of each of these types of growths was inherited.     

Changes in the timing of mantle formation and larval life history traits in linguliform and craniiform brachiopods

The distribution of embryonic and larval mantles is documented in linguliform and craniiform brachiopods. Criteria are presented for identifying these mantle types. The mantle type is related to planktotrophic and lecithotrophic larval life history patterns. In the Linguliformea and Craniiformea, all Lower Palaeozoic families with adequate preservation had larval mantles, indicating the presence of a planktotrophic larva. Heterochronic changes in the time of mantle origin, from the larval to the embryonic stage of development, has occurred several times. In the Lingulidae this change appears to have taken place at about the time the family originated in the Devonian and has been retained in extant genera. The family Discinidae has also retained a planktotrophic larval stage from the Lower Palaeozic to the present. The extant genus Crania in the Craniidae has a short-lived lecithotrophic larva that lacks a mantle. Through the Lower Jurassic, this family had planktotrophic larvae with a larval shell. During the Upper Jurassic, genera with a lecithotrophic larva that lacked a larval shell began to appear; however, the last genera in this family with a planktotrophic larva and a larval shell did not become extinct until the Tertiary.     

Functional morphology of the mantle of Nautilus pompilius (Mollusca, Cephalopoda)

This study presents histological and cytological findings on the structural differentiation of the mantle of Nautilus pompilius in order to characterize the cells that are responsible for shell formation. The lateral and front mantle edges split distally into three folds: an outer, middle, and inner fold. Within the upper part of the mantle the mantle edge is divided into two folds only; the inner fold disappears where the hood is attached to the mantle. At the base of the outer fold of the lateral and front mantle edge an endo-epithelial gland, the mantle edge gland, is localized. The gland cells are distinguished by a distinct rough endoplasmic reticulum and by numerous secretory vesicles. Furthermore, they show a strong accumulation of calcium compounds, indicating that the formation of the shell takes place in this region of the mantle. Numerous synaptic contacts between the gland cells and the axons of the nerve fibers reveal that the secretion in the area of the mantle edge gland is under nervous control. The whole mantle tissue is covered with a columnar epithelium having a microvillar border. The analyses of the outer epithelium show ultrastructural characteristics of a transport active epithelium, indicating that this region of the mantle is involved in the sclerotization of the shell. Ultrastructural findings concerning the epithelium between the outer and middle fold suggest that the periostracum is formed in this area of the mantle, as it is in other conchiferan molluscs.     

Long-term dynamics and community structure of freshwater gastropods exposed to parasitism and other environmental stressors

1. Freshwater communities are subject to various abrupt environmental disturbances and increasing pollution levels in their habitat. According to the nature and the periodicity of disturbances (i.e. punctuated, recurrent or continuous), one may expect different kinds of response of the target gastropod communities. 2. The gastropod community of a French lake has been investigated for 10 years to study its responses to three main environmental disturbances: supra‐seasonal droughts, recurrent proliferations of cyanobacteria and parasitism by trematodes. The relationship between this latter factor, considered as a continuous stressor, and the gastropod community was a particular focus. 3. A total of 13 280 gastropods belonging to 17 species (mostly Pulmonata with Planorbidae as the dominant family) have been sampled in the lake over the 10‐year time series. Species composition of the gastropod community varied strongly during the study period as did species richness (0–14, mean of 6.5 ± 0.4 species) and abundance of gastropods (0–4456, mean of 192 ± 72 individuals). Trematode larvae belonging to 11 morphotypes of cercariae were detected in 15 of the 17 species of gastropods and had a total prevalence of 2.9%. 4. Droughts (punctuated stressor) were responsible for the disappearance of nearly all gastropod species, and thus represent a severe environmental stressor for them. Nevertheless, the extent of this stressor was limited since the gastropod community was highly resilient. 5. Recurrent proliferations of toxic cyanobacteria (recurrent stressor) coincided with the large decline of the gastropod community, corresponding to a strong decrease in abundance and species richness. Intoxication of gastropods by toxic cyanobacteria was demonstrated by the bioaccumulation of microcystins in all gastropod tissues. 6. Trematode parasitism (continuous stressor) did not affect the gastropod community despite the possibly strong impact of parasites on some host species (those with monthly prevalence as high as 100% at some times). Indeed, abundance and species richness of gastropods were scarcely influenced by trematode prevalence or species richness.     

Overcoming the constraints of spiral growth: the case of shell remodelling

As animals grow in size, their relationship to the physical environment necessarily changes, but molluscs and brachiopods whose accretionary skeletons expand at one end of a hollow cone conform to logarithmic-spiral growth and retain a constant shape. Dissolution and remodelling of previously formed parts of the skeleton can alleviate the constraints of strict logarithmic-spiral growth. How, when, where and in which clades mineral skeletal resorption has evolved are important questions because they relate to the conditions and history of skeletal formation and to the way in which ocean acidification in the past influenced that history. A synthesis of data on mineral dissolution in shells shows that resorption from the inner surface of bivalve shells occurs under temporarily anaerobic conditions within the closed shell, but functional remodelling is unknown in bivalves. Resorption and functional remodelling occur in brachiopods, gastropods and terrestrial hermit crabs, and to a lesser extent in scaphopods and cephalopods. Internal whorl resorption leading to a more compact visceral mass has evolved at least ten times in gastropods. Contrary to expectations stemming from patterns in the availability of calcium, gastropod remodelling is a phenomenon of warm, calcium-rich environments and not of cold acidified conditions. There is therefore no evidence that internal whorl resorption increases calcium-use efficiency. Resorption is one of several mechanisms that have enabled animal skeletons to become more dynamic and adaptable during ontogeny.     

Snails and their trails: the multiple functions of trail‐following in gastropods

Snails are highly unusual among multicellular animals in that they move on a layer of costly mucus, leaving behind a trail that can be followed and utilized for various purposes by themselves or by other animals. Here we review more than 40 years of experimental and theoretical research to try to understand the ecological and evolutionary rationales for trail‐following in gastropods. Data from over 30 genera are currently available, representing a broad taxonomic range living in both aquatic and terrestrial environments. The emerging picture is that the production of mucus trails, which initially was an adaptation to facilitate locomotion and/or habitat extension, has evolved to facilitate a multitude of additional functions. Trail‐following supports homing behaviours, and provides simple mechanisms for self‐organisation in groups of snails, promoting aggregation and thus relieving desiccation and predation pressures. In gastropods that copulate, trail‐following is an important component in mate‐searching, either as an alternative, or in addition to the release of water‐ or air‐borne pheromones. In some species, this includes a capacity of males not only to identify trails of conspecifics but also to discriminate between trails laid by females and males. Notably, trail discrimination seems important as a pre‐zygotic barrier to mating in some snail species. As production of a mucus trail is the most costly component of snail locomotion, it is also tempting to speculate that evolution has given rise to various ways to compensate for energy losses. Some snails, for example, increase energy intake by eating particles attached to the mucus of trails that they follow, whereas others save energy through reducing the production of their own mucus by moving over previously laid mucus trails. Trail‐following to locate a prey item or a mate is also a way to save energy. While the rationale for trail‐following in many cases appears clear, the basic mechanisms of trail discrimination, including the mechanisms by which many snails determine the polarity of the trail, are yet to be experimentally determined. Given the multiple functions of trail‐following we propose that future studies should adopt an integrated approach, taking into account the possibility of the simultaneous occurrence of many selectively advantageous roles of trail‐following behaviour in gastropods. We also believe that future opportunities to link phenotypic and genotypic traits will make possible a new generation of research projects in which gastropod trail‐following, its multitude of functions and evolutionary trade‐offs can be further elucidated.     

D-Aspartate oxidase and D-amino acid oxidase are localised in the peroxisomes of terrestrial gastropods

D-Aspartate oxidase and D-amino acid oxidase were found in high activity in the tissues of representative species of terrestrial gastropods. Analytical subcellular fractionation demonstrated that both of these oxidases co-localised with the peroxisome markers, acyl-CoA oxidase and catalase, in the digestive gland homogenate. Electron microscopy of peak peroxisome fractions showed particles of uniform size with generally well preserved variably electron-dense matrices bounded by an apparently single limiting membrane. Many of the particles exhibited a core region of enhanced electron density. Catalase cytochemistry of peak fractions confirmed the peroxisome identity of the organelles. Peroxisome-enriched subcellular fractions were used to investigate the properties of gastropod D-aspartate oxidase and D-amino acid oxidase activities. The substrate and inhibitor specificities of the two activities demonstrated that two distinct enzymes were present analogous to, but not identical to, the equivalent mammalian peroxisomal enzymes.     

The outer mantle epithelium of Haliotis tuberculata (Gastropoda Haliotidae): an ultrastructural and histochemical study using lectins

The mantle of molluscs has been the subject of many studies as it is the organ that forms the shell. Microscopic studies in particular focus on the outer mantle epithelium, but few studies address this epithelium in a histochemical way. In this study, the outer mantle epithelium in adult specimens of Haliotis tuberculata is studied, that is, in specimens involved in maintaining and repairing the shell rather than in generating it. The epithelial cells are studied by scanning (SEM) and transmission electron microscopy (TEM), and by histochemical techniques, including the use of lectins for their biochemical characterization. The epithelium is composed of pigmented epidermal cells with small microvilli and junctional complexes. It furthermore contains a few ciliated cells, as well as two types of secretory cells which differ in the ultrastructural appearance of their secretory granules and their glycoconjugate content. Histochemical study shows secretory cells containing sulphated glycoconjugates such as glycosaminoglycans or mucins rich in N‐acetylgalactosamine and N‐glycoproteins rich in fucose. Furthermore, the apical regions of the epidermal cells are positive for lectins that label fucose, mannose and N‐acetylglucosamine. The role of epithelial cells in the synthesis of structural components of the shell is discussed.     

Magnetically induced electric fields and currents in the circulatory system

Blood flow in an applied magnetic field gives rise to induced voltages in the aorta and other major arteries of the central circulatory system that can be observed as superimposed electrical signals in the electrocardiogram (ECG). The largest magnetically induced voltage occurs during pulsatile blood flow into the aorta, and results in an increased signal at the location of the T-wave in the ECG. Studies involving the measurement of blood pressure, blood flow rate, heart sounds, and cardiac valve displacements have been conducted with monkeys and dogs exposed to static fields up to 1.5 tesla (T) under conditions producing maximum induced voltages in the aorta. Results of these studies gave no indication of alterations in cardiac functions or hemodynamic parameters. Cardiac activity monitored by ECG biotelemetry during continuous exposure of rats to a 1.5-T field for 10 days gave no evidence for any significant changes relative to the 10 days prior to and following exposure. Theoretical modeling of magnetic field interactions with blood flow has included a complete solution of the equation describing the flow of an electrically conductive fluid in the presence of a magnetic field (the Navier–Stokes equation) using the finite element technique. Magnetically induced voltages and current densities as a function of the applied magnetic field strength have been calculated for the aorta and surrounding tissues structures, including the sinoatrial node. Induced current densities in the region of the sinoatrial node are predicted to be >100 mA/m² at field levels >5 T in an adult human under conditions of maximum electrodynamic coupling with aortic blood flow. Magnetohydrodynamic interactions are predicted to reduce the volume flow rate of blood in the human aorta by a maximum of 1.3%, 4.9%, and 10.4% at field levels of 5, 10, and 15 T, respectively.     

Land hermit crab (Coenobita clypeatus) densities and patterns of gastropod shell use on small Bahamian islands

Aim To examine patterns of abundance, density, size and shell use in land hermit crabs, Coenobita clypeatus (Herbst), occurring on three groups of small islands, and to determine how these variables change among islands. Location Small islands in the Central Exuma Cays and near Great Exuma, Bahamas. Methods Land hermit crabs were captured in baited pitfall traps and were separately attracted to baits. A mark–recapture technique was used in conjunction with some pitfall traps monitored for three consecutive days. The size of each crab and the type of adopted gastropod shell were recorded, along with physical island variables such as total island area, vegetated area, island perimeter, elevation and distance to the nearest mainland island. Results Relative abundances, densities and sizes of crabs differed significantly among the three island groups. Densities of land hermit crabs were as high as 46 m⁻² of vegetated island area. In simple and multiple linear regressions, the only variable that was a significant predictor of the abundance of hermit crabs was the perimeter to area ratio of the island. Patterns of gastropod shell use varied significantly among the island groups, and the vast majority of adopted shells originated from gastropod species that inhabit the high intertidal and supratidal shorelines of the islands. Main conclusions Although densities of land hermit crabs varied, they were relatively high on many islands, and land hermit crabs may play an important role in these insular food webs. Patterns of shell use may be strongly restricted by island geomorphology: irregular shorelines provide relatively more habitat for the gastropod species that account for the majority of adopted shells and the steep sides of the islands prevent the accumulation of marine gastropod shells. The size of adult hermit crabs appears to be limited by the relatively small gastropod shells available, while the abundance of hermit crabs may be limited by the number of shells available.     

The effect of water exchange on bacterioplankton depletion and inorganic nutrient dynamics in coral reef cavities

We studied the effect of water exchange on the depletion (or accumulation) of bacterioplankton, dissolved organic matter and inorganic nutrients in small open framework cavities (50–70 l) at 15 m depth on the coral reef along Curaçao, Netherlands Antilles. The bacterioplankton removal rate in cavities increased with increasing water exchange rates up to a threshold of 0.0045 s⁻¹, reaching values of 50–100 mg C m⁻² total interior cavity surface area (CSA) per day. Beyond the threshold, bacterioplankton removal dropped. The cryptic community is apparently adapted to the average water exchange in these cavities (0.0041 s⁻¹). Dissolved inorganic nitrogen (DIN), nitrate + nitrite (NO _x ) in particular, accumulated in cavity water and the accumulation decreased with increasing water exchange. Net NO _x effluxes exceeded net DIN effluxes from cavities (average efflux rate of 1.9 mmol NO _x vs. 0.8 mmol DIN m⁻² interior CSA per day). The difference is ascribed to net ammonium losses (NH₄) in cavities at reef concentrations >0.025 μM NH₄, possibly due to enhanced nitrification. Dissolved inorganic phosphate accumulated in cavities, but was not related to water exchange. The cryptic biota in cavities depend on water exchange for optimization of consumption of bacterioplankton and removal of inorganic nitrogen. Coral cavities are an evident sink of bacterioplankton and a source of NO _x and PO ₄ ³⁻ .     

Paleobiological implications of shell repair in recent marine gastropods from the northern Gulf of California

Shell repair frequencies in eleven species of Recent gastropods from the northern Gulf of California vary with habitat, shell morphology and intensity of durophagous predation. Squat shells with large apertures tend to have high repair frequencies (0.25–0.50). Shell thickness at the aperture and shell size are not correlated with frequency of repair. Significant intraspecific variation in repair frequency exists between habitats. Samples from rocky habitats have statistically higher repair frequencies than samples of the same species from sandy habitats. However, habitat‐related variation between species is not apparent.

Trends in co‐evolution of gastropods and their durophagous predators are based on the indirect evidence of shell repair frequencies through time. Variation in repair frequency due to environmental and morphological factors may obscure predator‐related temporal trends in repair frequency.     

Dynamics of water molecules buried in cavities of apolipoprotein E studied by molecular dynamics simulations and continuum electrostatic calculations

Molecular dynamics (MD) simulations of several nanoseconds each were used to monitor the dynamic behavior of the five crystal water molecules buried in the interior of the N-terminal domain of apolipoprotein E. These crystal water molecules are fairly well conserved in several apolipoprotein E structures, suggesting that they are not an artifact of the crystal and that they may have a structural and/or functional role for the protein. All five buried crystal water molecules leave the protein interior in the course of the longest simulations and exchange with water molecules from the bulk. The free energies of binding evaluated from the electrostatic binding free energy computed using a continuum model and estimates of the binding entropy changes represent shallow minima. The corresponding calculated residence times of the buried water molecules range from tens of picoseconds to hundreds of nanoseconds, which denote rather short times as for buried water molecules. Several water exchanges monitored in the simulations show that water molecules along the exit/entrance pathway use a relay of H bonds primarily formed with charged residues which helps either the exit or the entrance from or into the buried site. The exit/entrance of water molecules from/into the sites is permitted essentially by local motions of, at most, two side chains, indicating that, in these cases, complex correlated atomic motions are not needed to open the buried site toward the surface of the protein. This provides a possible explanation for the short residence times.     

Streptococcus panodentis sp. nov. from the oral cavities of chimpanzees

Three strains TKU9, TKU49 and TKU50^T, were isolated from the oral cavities of chimpanzees (Pan troglodytes). The isolates were all gram‐positive, facultative anaerobic cocci that lacked catalase activity. Analysis of partial 16S rRNA gene sequences showed that the most closely related species was Streptococcus infantis (96.7%). The next most closely related species to the isolates were S. rubneri, S. mitis, S. peroris and S. australis (96.6 to 96.4%). Based on the rpoB and gyrB gene sequences, TKU50^T was clustered with other member of the mitis group. Enzyme activity and sugar fermentation patterns differentiated this novel bacterium from other members of the mitis group streptococci. The DNA G + C content of strain TKU50^T was 46.7 mol%, which is the highest reported value for members of the mitis group (40–46 mol%). On the basis of the phenotypic characterization, partial 16S rRNA gene and sequences data for two housekeeping gene (gyrB and rpoB), we propose a novel taxa, S. panodentis for TKU 50^T (type strain = CM 30579^T = DSM 29921^T), for these newly described isolates.     

Temporal and spatial patterns in the recruitment of Gibbula umbilicalis

Size/frequency samples have been taken from populations of the trochid gastropod Gibbula umbilicalis at a number of sites around the British Isles each year since 1978. In the North of Scotland, close to the limit of the species distribution, recruitment was generally poor and populations were sparse and dominated by large old individuals. While such poor recruitment may reflect the low density of adults and the shortage of nursery areas, a distinct temporal pattern of recruitment was also evident. At the start of our study, the majority of sites had population structures biased towards young animals implying that conditions for the settlement of larvae or their subsequent survival had been favourable over a wide area. In the years that followed only the enclosed Loch Eriboll regularly received substantial recruitment. Further to the south, in Wales and S.W. England, recruitment was usually more regular, populations were more dense and individuals smaller.