Development and evolution of adult feeding structures in Caenogastropods: overcoming larval functional constraints

SUMMARY Comparative study of the developing foregut in three species of caenogastropods, including an herbivorous grazer ( Lacuna vincta ) and two carnivores ( Euspira [ Polinices ] lewisii and Nassarius mendicus ), suggests how the specialized adult foregut of a carnivorous neogastropod evolved within a life cycle having a planktotrophic larva. Postmetamorphic feeding structures (buccal cavity and radular sac) in all three species achieve advanced differentiation in the larval stage, permitting juvenile feeding at 3 days postmetamorphosis. Recent phylogenetic hypotheses for the Gastropoda predict that foregut developmental patterns in E. lewisii and N. mendicus are derived, relative to that of L. vincta. In hatching larvae of these three, the anlage of postmetamorphic feeding structures is a small patch of nonciliated cells embedded in the ventral wall of the larval foregut and the patch soon forms an outpocketing. During subsequent morphogenesis, Euspira lewisii and N. mendicus share a developmental novelty that involves semi-isolation of the developing, postmetamorphic buccal cavity and radular sac from the larval foregut and formation of a new, definitive mouth at metamorphosis. Nassarius mendicus , a neogastropod, embellishes this novelty by adding the entire anterior esophagus and valve of Leiblein ( de novo structures) to the semi-isolated buccal cavity. Therefore, a valve and long stretch of muscular anterior esophagus, which are necessary for feeding with a pleurembolic proboscis, are preformed in the larval stage of this neogastropod without interfering with larval feeding. The inferred evolutionary events leading to postmetamorphic feeding specialization in N. mendicus are invisible in adults; they require reconstruction from comparative developmental analysis.     

THE ONTOGENY OF THE PLEUREMBOLIC PROBOSCIS IN NUCELLA LAPILLUS (GASTROPODA: MURICIDAE)

The ontogeny of the proboscis in Nucclla lapillus was investigatedusing light and scanning electron microscopy. The proboscis develops by elongation of the body wall surroundingthe mouth, whilst the rhynchocoel is formed by imagination ofthe body wall surrounding the proboscis. Elongation of the snoutduring development of the proboscis results in the anteriormovement of the anterior oesophagus and part of the mid-oesophagus(the valve of Leiblein) which is drawn through the circum-oesophagealnerve ring. The acinous salivary glands and the radular sacalso come to lie anterior to the nerve ring. The mid-oesophagealgland of Leiblein and the glandular dorsal folds are not drawnthrough the nerve ring, and develop behind it. The anterioroesophagus elongates at a later stage of development to producethe oesophageal length required for extension of the adult proboscis.Modifications to this sequence of events, or changes in therate of growth of the various parts of the foregut, might accountfor the differences between the neogastropod and neotaenioglossanpleurembolic proboscis. The intraembolic proboscis found inthe Conoidea and the Pseudolivoidea may have been derived viaa modification of the developmental sequence which producesthe muricoidean pleurembolic proboscis. (Received 10 May 1996; accepted 15 August 1996)     

Metamorphic remodeling of a planktotrophic larva to produce the predatory feeding system of a cone snail (Mollusca, Neogastropoda)

I used histological sections and 3D reconstructions to document development through metamorphosis of the foregut and proboscis in the conoidean neogastropod Conus lividus. A goal was to determine how highly derived features of the post-metamorphic feeding system of this gastropod predator develop without interfering with larval structures for microherbivory. A second goal was to compare foregut development in this conoidean with previous observations on foregut development in the buccinoidean neogastropod Nassarius mendicus. These two neogastropods both have a feeding larval stage, but they show major differences in post-metamorphic foregut morphology. Basic events in development of the proboscis and proboscis sheath in C. lividus and N. mendicus were similar. However, the elongate buccal tube of C. lividus forms during metamorphosis as a composite of apical epidermal tissue that grows inward and ventral foregut tissue that extends outward. The larval mouth is not carried through metamorphosis. Comparative observations on foregut development in caenogastropods, which now include data on C. lividus, suggest that the foregut incorporates dorsal and ventral modules having different ontogenetic and functional fates. This developmental modularity may have facilitated evolutionary diversification of the post-metamorphic foregut. Foregut diversification in predatory gastropods may have been further fast-tracked by developmental uncoupling of larval and post-metamorphic mouths.     

Feeding of the Cymatiid Gastropod, Argobuccinum argus, in Relation to the Structure of the Proboscis and Secretions of the Proboscis Gland

Several gastropod families belonging to the superfamily Tonnaceaare known to bore into the calcareous shells of echinoids andbivalves, but little work has been done on the family Cymatiidae.New observations show that the cymatiid, Argobuccinum argus,which feeds on the tubicolous polychaete, Gunnarea capensis,possesses large proboscis glands which secrete 0.4 to 0.5N H₂SO₄;further, the secretion dissolves greater amounts of pure CaCO₃than does O.47N H₂SO₄, alone. A toxin is also present, whichabolishes responses to light and touch in several invertebrates. The proboscis is atypically pleurembolic, having a permanentproboscis sheath. Retraction is due to the muscles ot the probosciswall, and the contracted proboscis is not inverted. Unlike othermesogastropods, the Tonnacea have three pairs ofglands associatedwith the foregut: proboscis glands, true salivary glands, anda small, partly paired gland of unknown function immediatelyposterior to the buccal mass. It is concluded that because of an abundance of readily availablefood in the form of Gunnarea, A. argus does not drillinto animalsprotected by a calcareous shell. The presence of a CaCO₃ dissolvingmechanism indicates that the Cymatiidae ingeneral may be ableto employ this method of feeding.     

On the hoplonemertean Sagaminemertes nagaiensis (Iwata, 1957), with consideration of its systematics

Summary The polystiliferous hoplonemertean Sagaminemertes nagaiensis (Iwata, 1957) has been redescribed.A distinct pre-cerebral region is wanting. The rhynchocoel opens directly at the tip of the head, whilst the mouth opens seperately below the ventral commissure of the brain which is situated at the anterior end of the head. The dorsal ganglia are well developed and extend posteriorly far behind the ventral ganglia. The cerebral sense organs are situated behind the brain and possess posterior ciliated canals. Cephalic glands are poorly represented, but ocelli are well developed. The sickle-shaped basis of the proboscis bears about 20 central stylets. The caecal appendages of the rhynchocoel are arranged pseudometamerically throughout the body. The foregut is straight, consisting of mouth, oesophagus, stomach and pylorus. Intestinal caeca and lateral diverticula are present. The cephalic lacunae have no anterior anastomosis. A cerebral lacuna is present, there is a rhynchocoel vessel, but transverse vessels are absent. The protonephridia extend throughout the foregut region. Mature spermatogonia are well developed.A systematic discussion of Sagaminemertes nagaiensis suggests that it is taxonomically close to Siboganemertes weberi in the archireptantic family Siboganemertidae.     

Ultrastructure of the labrum and foregut of Derocheilocaris remanei (Crustacea,Mystacocarida)

The cuticle-lined foregut of Derocheilocaris remanei consists of the mouth with its associated labrum, and an undifferentiated esophagus. It is separated from the midgut by an esophageal valve. The labrum is a conspicuous structure moved by five pairs of muscles (four dorsoventral and one longitudinal). Four pairs of subcuticular glands open to its inner face forming two longitudinal, lateral rows of cuticular pores. Each secretory unit is composed of a glandular component (with one or two secretory cells), a neck cell, and a duct cell. In addition, a single gland cell opens mesially into the buccal cavity. The ventrally located mouth is a complex structure characterized by a filter-like system, a sensory organ, and epithelial cells with highly developed microvilli. The esophagus is a simple tube with a characteristic curvature following the mouth. It has a rounded cross section and a triradiate lumen. A layer of circular musculature surrounds this region. The end of the esophagus protrudes into the midgut lumen forming the so-called esophageal valve. The ultrastructural features of the foregut, with the presence of a mucus-trapping mechanism, a relatively well-developed filter system and associated structures and an esophagus lacking glands confirm the microphagic feeding habits of mystacocarids. © 1996 Wiley-Liss, Inc.     

Feeding behaviour of a new worm (Priapulida) from the Sirius Passet Lagerstätte (Cambrian Series 2, Stage 3) of North Greenland (Laurentia)

Singuuriqia simoni gen. et sp. nov. represents the first record of a priapulid worm from the Sirius Passet Lagerstätte (Cambrian Series 2, Stage 3) of North Greenland (Laurentia). It is defined by an unusually broad, longitudinally folded, foregut which tapers through the pharynx towards the anterior mouth; posteriorly, the same longitudinal folding is evident in the narrow gut. The slender, smooth, trunk in the unique specimen passes anteriorly into an oval proboscis which culminates in a smooth, extensible, pharynx with pharyngeal teeth. The capacity for substantial expansion of the foregut permitted rapid ingestion of food prior to digestion at leisure. Cololites suggest both carnivorous and deposit feeding behaviour, indicating that Singuuriqia, like the present day Priapulus, was probably omnivorous.     

Functional adaptations of the digestive system of the carnivorous mollusc Pleurobranchaea californica MacFarland, 1966

The opisthobranch mollusc Pleurobranchaea californica feeds on whole organisms and the functional morphology of the digestive system reflects this behavior. By a rhythmic behavior involving well-developed extrinsic buccal muscles and hemocoelic fluid, the buccal mass is protracted to the tip of the everted oral tube. Here a series of repeated protractions and retractions of the intrinsic buccal muscles associated with the flat radular ribbon and jaws draws the prey into the buccal cavity and conveys it to the dorsal esophagus, where by peristaltic action it is passed to the expansible crop for storage. Prey entering the buccal cavity is mixed with acid from a large single gland and secretion from the paired salivary glands. Prey is retained in the crop over long periods of time while it is slowly broken down and passed via the stomach into the digestive glands. Special modifications that allow flexibility of the digestive organs include elongated salivary gland ducts with propulsive bulbs, long flexible nerve cords connecting the ganglia, a long, large muscular duct for storage of the acid secretion, large jaws for muscle attachment and grasping the prey, and a broad radular ribbon with many teeth that acts as a conveyor belt to move food. Additional modifications for handling whole prey include a buccal membrane that aids in maintaining hemocoelic fluid pressure, the extensive acid gland for immobilization of prey, and the expansible crop for storage of food.     

Morphological specializations of the buccal cavity in relation to the food and feeding habit of a carp Cirrhinus mrigala: A scanning electron microscopic investigation

The buccal cavity of an herbivorous fish, Cirrhinus mrigala, was investigated by scanning electron microscopy to determine its surface ultrastructure. The buccal cavity shows significant adaptive modifications in relation to food and feeding ecology of the fish. The buccal cavity of the fish is of modest size and limited capacity, which is considered an adaptation with respect to the small‐sized food items primarily consumed by the fish that could be accommodated in a small space. Modification of surface epithelial cells, on the upper jaw, into characteristic structures—the unculi—is considered an adaptation to browse or scrap, to grasp food materials, e.g., algal felts, and to protect the epithelial surface against abrasions, likely to occur during their characteristic feeding behavior. Differentiation of the highly specialized lamellar organ on the anterior region of the palate could be an adaptation playing a significant role in the selection, retention, and sorting out of palatable food particles from the unpalatable items ingested by the fish. The filamentous epithelial projections and the lingulate epithelial projections on the palatal organ in the posterior region of the palate are considered to serve a critical function in final selection, handling, maneuvering, and propelling the food particles toward the esophagus. The abundance of different categories of taste buds in the buccal cavity suggests that gustation is well developed and the fish is highly responsive in the evaluation and the selection of the preferred palatable food items. The secretions of mucous cells in the buccal cavity are associated with multiple functions—particle entrapment, lubrication of the buccal epithelium and food particles to assist smooth passage of food, and to protect the epithelium from possible abrasion. These morphological characteristics ensure efficient working of the buccal cavity in the assessment of the quality and palatability of ingested food, their retention and transport toward the esophagus. Such an adaptation may be essential in conducting the function most basic to the survival of the individuals and species—feeding. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

Evidence for homologous peptidergic neurons in the buccal ganglia of diverse nudibranch mollusks

The buccal ganglia of seven nudibranches (Aeolidia papillosa, Armina californica, Dirona albolineata, D. picta, Hermissenda crassicornis, Melibe leonina, and Tritonia diomedea) were examined to explore possible homologies between large cells that reacted with antibodies directed against small cardioactive peptide B (SCP_B). The buccal ganglion of each species possessed a pair of large, dorsal–lateral, whitish neurons that contained an SCP_B-like peptide. We refer to these neurons as the SLB (SCP_B-immunoreactive Large Buccal) cells. In all species examined, the SLB cells project out the gastroesophageal nerves and appear to innervate the esophagus. In each species, an apparent rhythmic feeding motor program (FMP) was observed by intracellular recording from both SLB neurons and other neurons in isolated preparations of the buccal ganglia. SLB cells often fire at a high frequency, and usually burst in a specific phase relation to the FMP activity. Stimulation of SLB cells enhances expression of the feeding motor program, either by potentiating existing activity or eliciting the FMP in quiescent preparations. Finally, perfusion of isolated buccal ganglia with SCP_B excites the SLB cells and activates FMPs. Thus, both the immunohistochemical and electrophysiological data suggest that the SLB cells within three suborders of the opistobranchia (Dendronotacea, Arminacea, and Aeolidacea) are homologous. A comparison of our data with previously published studies indicates that SLB cell homologs may exist in other gastropods as well.     

Ultrastructure of the foregut and associated glands in the lung fluke,Paragonimus miyazakii (Digenea: Troglotrematidae), with particular reference to their functional roles

The foregut and associated glands of a digenetic trematode, Paragonimus miyazakii, were examined in the forebody by transmission and scanning electron microscopy as well as by light microscopy, and their functional roles were discussed. The foregut is lined with a general tegument without spines and sensory receptors throughout its length, although it consists of the mouth, pharynx, and esophagus. This foregut tegument is regionally and intraregionally modified in appearance, suggesting the performance of auxiliary functions in digestion. This appearance is characterized by long, frequent cytoplasmic extensions of the apical tegument around the middle portion of the mouth and the anterior esophagus. Electron-dense granules and multimembranous and multilamellar bodies are developed in the tegument to various degrees, and elaborately in the apical layer of the prepharynx. A single type of unicellular gland is embedded in the antero-middle part of the worm in small groups. The gland cells synthesize clear secretory granules as a chief product, each granule with a pleomorphic, dense, core-like inclusion. Mature granules are elliptical in shape, approximately 500 nm in diameter, and are subsequently discharged into the prepharyngeal foregut lumen after passing through the elongated cytoplasm of the gland cell. In the prepharynx and pharynx, host blood cells are apparently processed for digestion. In the wide lumen of the esophagus, foodstuff could undergo sufficient digestion prior to absorption by the cecal epithelium. J. Morphol. 237:43–52, 1998. © 1998 Wiley-Liss, Inc.     

Barx1-mediated inhibition of Wnt signaling in the mouse thoracic foregut controls tracheo-esophageal septation and epithelial differentiation

Mesenchymal cells underlying the definitive endoderm in vertebrate animals play a vital role in digestive and respiratory organogenesis. Although several signaling pathways are implicated in foregut patterning and morphogenesis, and despite the clinical importance of congenital tracheal and esophageal malformations in humans, understanding of molecular mechanisms that allow a single tube to separate correctly into the trachea and esophagus is incomplete. The homoebox gene Barx1 is highly expressed in prospective stomach mesenchyme and required to specify this organ. We observed lower Barx1 expression extending contiguously from the proximal stomach domain, along the dorsal anterior foregut mesenchyme and in mesenchymal cells between the nascent esophagus and trachea. This expression pattern exactly mirrors the decline in Wnt signaling activity in late development of the adjacent dorsal foregut endoderm and medial mainstem bronchi. The hypopharynx in Barx1^−/− mouse embryos is abnormally elongated and the point of esophago-tracheal separation shows marked caudal displacement, resulting in a common foregut tube that is similar to human congenital tracheo-esophageal fistula and explains neonatal lethality. Moreover, the Barx1^−/− esophagus displays molecular and cytologic features of respiratory endoderm, phenocopying abnormalities observed in mouse embryos with activated ß-catenin. The zone of canonical Wnt signaling is abnormally prolonged and expanded in the proximal Barx1^−/− foregut. Thus, as in the developing stomach, but distinct from the spleen, Barx1 control of thoracic foregut specification and tracheo-esophageal septation is tightly associated with down-regulation of adjacent Wnt pathway activity.     

Origin and segregation of cranial placodes in Xenopus laevis

Cranial placodes are local thickenings of the vertebrate head ectoderm that contribute to the paired sense organs (olfactory epithelium, lens, inner ear, lateral line), cranial ganglia and the adenohypophysis. Here we use tissue grafting and dye injections to generated fate maps of the dorsal cranial part of the non-neural ectoderm for Xenopus embryos between neural plate and early tailbud stages. We show that all placodes arise from a crescent-shaped area located around the anterior neural plate, the pre-placodal ectoderm. In agreement with proposed roles of Six1 and Pax genes in the specification of a panplacodal primordium and different placodal areas, respectively, we show that Six1 is expressed uniformly throughout most of the pre-placodal ectoderm, while Pax6, Pax3, Pax8 and Pax2 each are confined to specific subregions encompassing the precursors of different subsets of placodes. However, the precursors of the vagal epibranchial and posterior lateral line placodes, which arise from the posteriormost pre-placodal ectoderm, upregulate Six1 and Pax8/Pax2 only at tailbud stages. Whereas our fate map suggests that regions of origin for different placodes overlap extensively with each other and with other ectodermal fates at neural plate stages, analysis of co-labeled placodes reveals that the actual degree of overlap is much smaller. Time lapse imaging of the pre-placodal ectoderm at single cell resolution demonstrates that no directed, large-scale cell rearrangements occur, when the pre-placodal region segregates into distinct placodes at subsequent stages. Our results indicate that individuation of placodes from the pre-placodal ectoderm does not involve large-scale cell sorting in Xenopus.     

Praealbonemertes whangateaunienses n. gen. and n. sp., a new heteronemertean from New Zealand

Abstract

A new genus and species of heteronemertean, Praealbonemertes whangateaunienses n. gen. and n. sp., is described and illustrated. The species is characterised by inter alia a cephalic lacuna with strands of longitudinal muscle fibres, a proboscis with three muscle layers, and a well-developed muscle plate dorsal to the foregut and anterior intestine. The material was collected in New Zealand.     

Morphology of the anterior digestive system of tonnoideans (Gastropoda: Caenogastropoda) with an emphasis on the foregut glands

ABSTRACT

Tonnoideans are marine carnivorous caenogastropods that prey on different invertebrates, namely polychaetes, sipunculids, bivalve and gastropod molluscs, and echinoderms. The morphology of the digestive system of 20 species from five families of the Tonnoidea was examined (for most of these species for the first time), and the salivary glands of six of them were studied using serial histological sections. Most of the studied families are rather similar anatomically, except Personidae (Distorsio), which differs both in proboscis morphology and the structure of the salivary glands. In most tonnoideans the salivary glands are split morphologically and functionally into anterior and posterior lobes, the latter synthesising strong sulfuric acid. The ducts of the posterior lobes are lined with non-ciliated epithelium and receive usually paired ciliated ducts from the anterior lobes to form a non-ciliated common duct, opening into the buccal cavity. In Personidae, the salivary glands are not separated into lobes, but are instead composed of ramifying tubules that are histologically different in the proximal and distal parts. Radulae of Tonnoidea are rather variable, with different patterns of interlocking teeth, both in the transverse and longitudinal rows, which may be related to particular feeding mechanisms. Due to the peculiarities of Personidae, the close relationship between that family and the rest of the Tonnoidea is questioned.     

Studies on the tardigrades. I. Fine structure of the anterior foregut of Milnesium tardigradum Doyère

The fine structure of the anterior foregut of the tardigrade Milnesium tardigradum is presented. The oral region consists of a terminal mouth opening surrounded by six plate-like lips lying within a circlet of six prominent papillae. The buccal cavity is enclosed within a thick cuticular tube which possesses appendage structures, the stylet sheaths, stylet supports and paired protrusible stylets. Two large salivary glands envelop the buccal structures and contain voluminous amounts of secretory product. The arrangement, possible functions and phyletic significance of these structures are discussed.     

Neuropeptide TPep action on salivary duct ciliary beating rate in the nudibranch molluscTritonia diomedea

Recently, in the marine molluscTritonia, a family of three peptides (TPep-NLS,-PLS,-PAR) from identified pedal ganglion neurons has been characterized and shown to regulate ciliary beat frequency in epithelia and isolated cells of the molluscan foot. In this study, using an antiserum raised against TPep-NLS, immunofluorescent labelling was observed in specific nerve cell bodies and axons in the buccal ganglia ofTritonia, as well as in axons leading to and innervating the salivary ducts, salivary glands, oesophagus and foregut. This pattern of innervation suggests that buccal ganglion neurons containing TPep control the beating rate of ciliated cells in feeding organs. Accordingly, TPeps were introduced to isolated ciliated salivary ducts. It was found that TPeps and serotonin increased the ciliary beat frequency of cells of the salivary duct similarly; other peptides (such as APep fromAplysia) had no such effect. Threshold sensitivity both for TPeps and serotonin was approximately 10⁻⁸ M, with maximal response occurring above 10⁻⁵ M. Taken together, these structural and physiological results suggest that TPep-like peptides are present in the salivary and other feeding organs ofTritonia and are involved in the regulation of salivary transport.