THE PLANKTONIC VELIGER OF AMPHIBOLA CRENATA (GMELIN)

Amphibola crenata (Gmelin) has a well-developed planktonic veligerstage which remains in the plankton for several weeks and feedsactively. It resembles an opisthobranch veliger with a sinistralshell and conspicuous black larval kidney. After metamorphosisthe pitch of the coil of the shell is altered so that the bodywhorl grows, over the larval whorls and produces a dextrallycoiled adult shell with an internal protoconch. (Received 1 July 1980;     

Development of salinity tolerance in the marine pulmonate Amphibola crenata (Gmelin)

Growth and survival of veligers of Amphibola crenata (Gmelin) were followed in a range of salinities from 4 to 35%. In salinities of 18%. and below, growth was slowed and a large proportion of veligers died. In 4 to 12%., no larvae survived to metamorphosis, but these low salinities were tolerated for short periods.Newly post-metamorphic snails and juveniles collected from the field survived well even at 4%., showing that greater tolerance of low external salinities developed at metamorphosis. Examination of the physiology of adult snails suggested that this may be due to the development of osmoregulating mechanisms, because the adults maintain the blood hyperosmotic to the medium in 4 and 9%. The kidney, however, does not seem to be involved in this regulation because urine is isosmotic with the blood. An extra-renal mechanism of salt uptake is, therefore, postulated.     

Eastward and Westward Dispersal Across the Tropical Atlantic Ocean of Larvae Belonging to the Genus Bursa (Prosobranchia,Mesogastropoda, Bursidae)

Larvae of the genus Bursa are commonly found in the South Equatorial Current and the Equatorial Undercurrent of the tropical Atlantic Ocean. Identification of Bursa veliger larvae in the plankton of such tropical waters is made possible by a comparison of larval shells with protoconchs of juvenile and well-preserved adult specimens. The relationship between the average current velocity and the estimated minimum duration of larval development of Bursa thomae suggests that there is sufficient time to account for successful trans-Atlantic transport of its veligers in either direction between West Africa and South America. The dispersal of veliger larvae explains the wide geographical distribution attained by the genus Bursa.     

Apical sensory organ in larvae of the patellogastropod Tectura scutum

The apical sensory organ in veliger larvae of a patellogastropod, a basal clade of gastropod molluscs, was studied using ultrastructural and immunohistochemical techniques. Immediately before veligers of Tectura scutum undergo ontogenetic torsion, the apical sensory organ consists of three large cells that generate a very long apical ciliary tuft, two cells that generate a bilateral pair of shorter ciliary tufts, and a neural ganglion (apical ganglion). Putative sensory neurons forming the ganglion give rise to dendrites that extend to the apical surface of the larva and to basal neurites that contribute to a neuropil. The ganglion includes only one ampullary neuron, a distinctive neuronal type found in the apical ganglion of other gastropod veligers. Serotonin immunoreactivity is expressed by a medial and two lateral neurons, all having an apical dendrite, and also by neurites within the neuropil and by peripheral neurites that run beneath the ciliated prototrochal cells that power larval swimming. The three cells generating the long apical ciliary tuft are lost soon after ontogenetic torsion, and the medial serotonergic cell stops expressing serotonin antigenicity in late-stage veligers. The lateral ciliary tuft cells of T. scutum may be homologs of lateral ciliary tuft cells in planktotrophic opisthobranch veligers. A tripartite arrangement of sensory dendrites, as described previously for veligers of other gastropod clades, can be recognized in T. scutum after loss of the apical ciliary tuft cells.     

Myogenesis in Aplysia californica (Cooper, 1863) (Mollusca,Gastropoda, Opisthobranchia) with special focus on muscular remodeling during metamorphosis

To date only few comparative approaches tried to reconstruct the ontogeny of the musculature in invertebrates. This may be due to the difficulties involved in reconstructing three dimensionally arranged muscle systems by means of classical histological techniques combined with light or transmission electron microscopy. Within the scope of the present study we investigated the myogenesis of premetamorphic, metamorphic, and juvenile developmental stages of the anaspidean opisthobranch Aplysia californica using fluorescence F‐actin‐labeling in conjunction with modern confocal laser scanning microscopy. We categorized muscles with respect to their differentiation and degeneration and found three true larval muscles that differentiate during the embryonic and veliger phase and degenerate during or slightly after metamorphosis. These are the larval retractor, the accessory larval retractor, and the metapodial retractor muscle. While the pedal retractor muscle, some transversal mantle fibers and major portions of the cephalopedal musculature are continued and elaborated during juvenile and adult life, the buccal musculature and the anterior retractor muscle constitute juvenile/adult muscles which differentiate during or after metamorphosis. The metapodial retractor muscle has never been reported for any other gastropod taxon. Our findings indicate that the late veliger larva of A. californica shares some common traits with veligers of other gastropods, such as a larval retractor muscle. However, the postmetamorphic stages exhibit only few congruencies with other gastropod taxa investigated to date, which is probably due to common larval but different adult life styles within gastropods. Accordingly, this study provides further evidence for morphological plasticity in gastropod myogenesis and stresses the importance of ontogenetic approaches to understand adult conditions and life history patterns. J. Morphol., 2008. © 2007 Wiley‐Liss, Inc.     

HOMOLOGY OF THE PALLIAL AND PULMONARY CAVITY OF GASTROPODS

The development and morphology of the pallial and pulmonarycavities of various gastropods has been investigated using epoxy-resinserial sections. In the veliger larvae of Cellana sandwicensis(Patellogastro-poda), Gibbula adansonii (Vetigastropoda), Modulustectum (Caenogastropoda) and Ovatella myosotis (Pulmonata) theformation of the pallial cavity is nearly identical. After shellformation a shallow dorsal pallial groove develops beneath themantle edge. During the late veliger stage, the ectoderm formsa deep invagination along the bottom of the pallial groove onthe right side of the larva, giving rise to the pallial cavity.In the ellobiid O. myosotis the pallial cavity becomes the lung(=pulmonary cavity), without any major post-metamorphic modification.Thus, the lung of this species is clearly homologous with thepallial cavity of prosobranchs. The lung of pulmonates withveliger development, as well as of fresh water basommatophoransand stylommatophorans, can be shown to be homologous by comparisonof adult morphology. In contrast to previous views, the pulmonatelung should be regarded as truly homologous with the pallialcavity of prosobranchs and opisthobranchs. In the onchidiidpulmonate Onchidium cf. branchiferum, the larval pallial cavityshifts posteriorly after metamorphosis, where it gives riseto a lung and a cloaca. Contrary to previous interpretations,it can be shown that the onchidiid lung is homologous with atleast part of the pallial cavity. Smeagol climoi has only asmall pallial cavity and no separate lung. The previously described‘lung’ is shown to be a gland. The re-evaluationof the development and morphology of the pulmonate lung hasimportant systematic implications: (1) The pulmonary cavitydoes not represent a synapomorphic character of pulmonates.(2) The gymnomorphs cannot be separated from the remaining pulmonatesbased on lung development. (3) The lack of a lung in the smeagolidsmight give reason to reconsider this group's systematic placementwithin the pulmonates.     

Veligers of an introduced bivalve,Limnoperna fortunei,are a new food resource that enhances growth of larval fish in the Paraná River (South America)

1. Larvae of ‘sábalo’, Prochilodus lineatus, whose adults represent over 60% of overall fish biomass in the Río de la Plata Catchment, have been observed to feed intensively on veligers of the exotic bivalve Limnoperna fortunei. 2. To assess the effects of this dietary shift on the growth of P. lineatus, 28‐day laboratory experiments were carried out feeding newly hatched P. lineatus larvae with three diets: zooplankton artificially enriched with L. fortunei veligers; natural zooplankton; and zooplankton artificially enriched with cladocerans and copepods. The average length, weight and gut contents of the fish larvae were assessed weekly and metabolic rates of fish larvae were measured. 3. Proportions of veligers in gut contents were always higher than those in the experimental diet: 100, 76 and 21% for veliger‐enriched, natural and low‐veliger diets, respectively. Larvae fed a veliger‐enriched diet grew to a significantly larger size than larvae fed the other two diets. In energetic balance comparisons using metabolic rates and prey energy content, all three diets were sufficient to support metabolism and growth. The greatest values of excess energy at the end of each week were in the veliger‐enriched experiments. 4. Feeding on veligers of L. fortunei significantly enhances the growth of P. lineatus larvae and supports the idea that this new and abundant resource is selectively preyed upon by P. lineatus during its larval stage. Higher growth rates may stem from the higher energy contents of veligers compared to crustaceans and/or from the lower energy costs of capturing slower prey.     

Larval development and metamorphosis in Pleurobranchaea maculata, with a review of development in the notaspidea (Opisthobranchia)

Pleurobranchaea maculata is a carnivorous notaspidean that is common in New Zealand. This species produces small eggs (diameter 100 microm) and planktotrophic veligers that hatch in 8 d and are planktonic for 3 weeks before settling on biofilmed surfaces (14 degrees C). Larval development is known in detail for only two other notaspidean species, P. japonica and Berthellina citrina. In all three species of pleurobranchids, mantle and shell growth show striking differences from veligers of other opisthobranch taxa. In young veligers of pleurobranchids, the shell is overgrown by the mantle, new shell is added by cells other than those of the mantle fold, and an operculum does not form. Thus some "adult" traits (e.g., notum differentiation, mechanism of shell growth, lack of operculum) are expressed early in larval development. This suggests that apomorphies characteristic of adult pleurobranchids evolved through heterochrony, with expression in larvae of traits typical of adults of other clades. The protoconch is dissolved post-settlement and not cast off as occurs in other opisthobranch orders, indicating that shell loss is apomorphic. P. maculata veligers are atypical of opisthobranchs in having a field of highly folded cells on the lower velar surface, a mouth that is posterior to the metatroch, and a richly glandular, possibly chemodefensive mantle. These data indicate that notaspidean larvae are highly derived in terms of the novel traits and the timing of morphogenic events. Phylogenetic analysis must consider embryological origins before assuming homology, as morphological similarities (e.g., shell loss) may have developed through distinct mechanisms.     

Siphonariid development: Quintessential euthyneuran larva with a mantle fold innovation (Gastropoda; Panpulmonata)

Recent phylogenetic revisions of euthyneuran gastropods (“opisthobranchs” and “pulmonates”) suggest that clades with a planktotrophic larva, the ancestral life history for euthyneurans, are more widely distributed along the trunk of the euthyneuran tree than previously realized. There is some indication that the planktotrophic larva of euthyneurans has distinctive features, but information to date has come mainly from traditional “opisthobranch” groups. Much less is known about planktotrophic “pulmonate” larvae. If planktotrophic larvae of “pulmonates” share unique traits with those of “opisthobranchs,” then a distinctive euthyneuran larval-type has been the developmental starting template for a spectacular amount of evolved morphological and ecological disparity among adult euthyneurans. We studied development of a siphonariid by preparing sections of larval and postmetamorphic stages for histological and ultrastructural analysis, together with 3D reconstructions and data from immunolabeling of the larval apical sensory organ. We also sought a developmental explanation for the unusual arrangement of shell-attached, dorso-ventral muscles relative to the mantle cavity of adult siphonariids. Adult siphonariids (“false limpets”) have a patelliform shell but their C-shaped shell muscle partially embraces a central mantle cavity, which is different from the arrangement of these components in patellogastropods (“true limpets”). It is not obvious how shell muscles extending into the foot become placed anterior to the mantle cavity during siphonariid development from a veliger larva. We found that planktotrophic larvae of Siphonaria denticulata are extremely similar to previously described, planktotrophic “opisthobranch” larvae. To emphasize this point, we update a list of distinctive characteristics of planktotrophic euthyneuran larvae, which can anchor future studies on the impressive evolvability of this larval-type. We also describe how premetamorphic and postmetamorphic morphogenesis of larval mantle fold tissue creates the unusual arrangement of shell-muscles and mantle cavity in siphonariids. This result adds to the known postmetamorphic evolutionary innovations involving mantle fold tissue among euthyneurans.     

Veligers from the nudibranch <Emphasis Type="Italic">Dendronotus</Emphasis><Emphasis Type="Italic">frondosus</Emphasis> show shell growth and extended planktonic period in laboratory culture

The planktonic period of planktotrophic veliger larvae from the nudibranch Dendronotus frondosus was characterized by laboratory culture methods. Larvae in culture successfully metamorphosed at 73–86 days after hatching. These veligers have Type 2 (Thompson) larval shells that significantly increased in length over the first 7–14 days after hatching. Direct observations of the development of nudibranch larvae with Type 2 protoconchs are limited, and these data help clarify previous attempts to correlate shell type and growth with minimum planktonic periods. Although these are not absolute values for the planktonic period of D. frondosus larvae, these data show the potential for extended larval dispersal and may help explain reports of an extensive geographic range in north-temperate waters for this species.     

Anti-tubulin labeling reveals ampullary neuron ciliary bundles in opisthobranch larvae and a new putative neural structure associated with the apical ganglion

This investigation examines tubulin labeling associated with the apical ganglion in a variety of planktotrophic and lecithotrophic opisthobranch larvae. Emphasis is on the ampullary neurons, in which ciliary bundles within the ampulla are strongly labeled. The larvae of all but one species have five ampullary neurons and their associated ciliary bundles. The anaspid Phyllaplysia taylori, a species with direct development and an encapsulated veliger stage, has only four ampullary neurons. The cilia-containing ampulla extends to the pretrochal surface via a long, narrow canal that opens to the external environment through a very small pore (0.1 microm diameter). Cilia within the canal were never observed to project beyond the opening of the apical pore. The ampullary canals extend toward and are grouped with the ciliary tuft cells and remain in this location as planktotrophic larvae feed and grow. If, as has been reported, the ciliary tuft is motile, the pores may be continually bathed in fresh seawater. Such an arrangement would increase sensitivity to environmental chemical stimuli if the suggested chemosensory function of these neurons is correct. In general, ciliary bundles of newly hatched veligers are smaller in planktotrophic larvae than in lecithotrophic larvae. In planktotrophic larvae of Melibe leonina, the ciliary bundles increase in length and width as the veligers feed and grow. This may be related to an increase in sensitivity for whatever sensory function these neurons fulfill. An unexpected tubulin-labeled structure, tentatively called the apical nerve, was also found to be associated with the apical ganglion. This putative nerve extends from the region of the visceral organs to a position either within or adjacent to the apical ganglion. One function of the apical nerve might be to convey the stimulus resulting from metamorphic induction to the visceral organs.     

Veligers of the invasive bivalve Limnoperna fortunei in the diet of indigenous fish larvae in a eutrophic subtropical reservoir

Larval fish development depends largely on their ability to capture and ingest food items, and on food availability. In this context, invasive species, eutrophication and river impoundments have complex impacts on fish larvae. Using samples collected in 2005–2009 in the Salto Grande reservoir (Argentina–Uruguay), periodically affected by cyanobacterial blooms, we studied the impact of the larvae of the exotic bivalve Limnoperna fortunei (Dunker, 1857) (Bivalvia) on larval fish diets. Compared with other nearby waterbodies, the abundance of fish larvae was scarcer in the reservoir, especially during algal bloom periods. Only 20% of the larval fish with gut contents fed on L. fortunei veligers. Seven fish taxa (of a total of 12) consumed veligers of L. fortunei, but only two showed a preference for this prey. Taxonomic changes in the larval fish assemblages due to the river's impoundment, and temporal uncoupling between veliger densities (affected by the toxigenic effects of Microcystis spp.) and ichthyoplankton could account for the comparatively low trophic importance of the invasive bivalve's veligers. These results reflect the complexity of interactions brought about when the same invasive species invades different environments, underscoring that the impacts involved depend as much on the invader, as on the regional and ecological settings of the area invaded.     

The biology of the Northeastern Pacific Turridae. V. Demersal development,synchronous settlement and other aspects of the larval biology of Oenopota levidensis

Summary

The larval development and metamorphosis of a turrid gastropod is described for the first time. This snail, Oenopota levidensis, is typical of the boreal genus Oenopota, which has over 150 described species. Development to a veliger occurs within a lenticular capsule in about 50 days. The capsules hatch to release veligers which swim for less than a week. The remainder of their planktotrophic larval period is spent demersally. Demersal veligers assumed one of two characteristic postures; they remain on the bottom with the velum either extended laterally or folded over the shell. These demersal veligers continue development and metamorphose after another 25 days. The majority of the veligers in the 55 cultures examined metamorphosed and settled within a 96-h period, even though their oviposition occurred over a 47-day period. Potential selective forces leading to this synchronous settlement are proposed.     

Parasite development and visceral pathology in Galba truncatula co-infected with Fasciola hepatica and Paramphistomum daubneyi

Histological investigations in Galba truncatula naturally or experimentally co-infected with Fasciola hepatica and Paramphistomum daubneyi were carried out to study parasite development and the responses of the digestive gland and kidney of snails, as larval forms of these digeneans often use these two sites for their growth within the snail's body. The number of live rediae per snail ranged from 2.4 to 4.2 for the dominating parasite (it developed in the digestive gland) and was less than 2.0 for the other species. When the dominating species was F. hepatica, most snails harboured cercariae-containing rediae; if this parasite was P. daubneyi, procercariae-containing rediae with or without free procercariae were observed in most snails. In contrast, most rediae of the other species were immature. The pathology caused by the dominating species in the digestive gland was greater than that recorded in the kidney, where the other parasite was generally located. The most frequent tissue lesions in the digestive gland were generalized epithelial necrosis and epithelial reconstitution. In the kidney, multifocal epithelial necrosis was frequently observed, particularly when P. daubneyi was the dominating species. The frequencies of lesions in the digestive gland agreed with percentages reported by our team in other snails mono-infected with F. hepatica or P. daubneyi. In contrast, multifocal necrosis in the kidney was clearly greater in the present study and this finding might be explained by assuming that a sufficient number of free larvae within the snail would be necessary for the development of epithelial necrosis in the whole kidney.     

The ecological and anatomy of a new species of aeolid opisthobranch mollusc; a predator of the scleractinian coral Porites

A new species of aeolid opisthobranch (family Tergipedidae) is described from Tanzania. It lives and feeds on the scleractinian coral Porites somaliensis. Studies on its development show that it can reach sexual maturity three weeks after hatching. The larval stage is extremely abbreviated; the veliger settles ten minutes after hatching, and within ninety minutes of hatching has assumed a slug-like form.     

Towards a ground pattern reconstruction of bivalve nervous systems: neurogenesis in the zebra mussel <Emphasis Type="Italic">Dreissena polymorpha</Emphasis>

Bivalvia is a taxon of aquatic mollusks that includes clams, oysters, mussels, and scallops. Within heterodont bivalves, Dreissena polymorpha is a small, mytiliform, freshwater mussel that develops indirectly via a planktotrophic veliger larva. Currently, only a few studies on bivalve neurogenesis are available, impeding the reconstruction of a ground pattern in Bivalvia. In order to inject novel data into this discussion, we describe herein the development of the serotonin-like and α-tubulin-like immunoreactive (lir) neuronal components of D. polymorpha from the early trochophore to the late veliger stage. Neurogenesis starts in the early trochophore stage at the apical pole with the appearance of one flask-shaped serotonin-lir cell. When larvae reach the veliger stage, four flask-shaped serotonin-lir cells are present in the apical organ. At the same time, the anlagen of the cerebral ganglia start to form at the base of the apical organ. From the apical organ, one pair of cerebro-visceral connectives projects posteriorly and connects to a posterior larval sensory organ that contains serotonin- and α-tubulin-like flask-shaped cells. Additional, paired serotonin-lir neurites originate from the apical organ and project into the velum. One unpaired stomatogastric serotonin-lir cell develops ventrally to the stomach at the veliger stage. The low number of serotonin-lir cells in the apical organ of bivalve veligers is shared with larvae of basally branching gastropods and scaphopods and is thus considered a feature of the last common ancestor of Conchifera, while the overall simplicity of the larval neural architecture appears to be a specific trait of Bivalvia.     

Downstream dispersal of zebra mussels (<Emphasis Type="Italic">Dreissena polymorpha</Emphasis>) under different flow conditions in a coupled lake-stream ecosystem

Dispersal, establishment, and spread of aquatic invasive species such as the zebra mussel (Dreissena polymorpha) can be influenced by riverine velocities and volumetric flows in invaded lake-stream ecosystems. Zebra mussels, which have a planktonic larval form (veliger), disperse rapidly downstream from a source population. Concentrations, dispersal, and body conditions of zebra mussel veligers were studied under different volumetric flow, or discharge, conditions in a coupled lake-stream ecosystem in northern Texas, USA. Veliger densities in lotic environments were strongly related to population dynamics in upstream lentic source populations. A strong exponential decrease in veliger density was observed through a 28-km downstream study reach. Increased water releases from the source reservoir increased veliger flux and dispersal potential, concomitantly increasing veliger flux and decreasing transit time. However, passage through release gates in the dam and increased turbulence in the river during high-discharge events could negatively affect body condition of veligers, and veliger body condition generally decreased from the source population to the farthest downstream site and was lower for veligers during periods of high discharge. Thus increased discharge appears to reduce the proportion of viable veligers because of increased turbulence-induced mortality. Colonization of distant downstream reservoirs can occur if discharge and propagule pressure are sufficient or if interim habitats are suitable for establishment of in-stream populations.     

Modulation of Mytilus trossulus (Bivalvia: Mollusca) larval survival and growth in culture. Short communication

Commercial importance and ability to live in a wide range of salinities have made the common mussel, Mytilus trossulus, a relevant model to study modulation of larval growth and development. We investigated the effects of various salinities combined with neomycin and ampicillin application on Mytilus larvae survival and growth. Both neomycin and ampicillin enhanced trochophore and veliger survival under condition of low salinity. The average veliger size was increasing in accordance with the increase of salinity. In case of neomycin treatment 3.6% of the larvae reached the pediveliger stage. No abnormalities of larval morphology of the FMRFamide and 5-HT systems occurred after 7 days of culturing with both antibiotics.     

Out-of-the tropics or trans-tropical dispersal? The origins of the disjunct distribution of the gooseneck barnacle Pollicipes elegans

Myogenesis is currently investigated in a number of invertebrate taxa using combined techniques, including fluorescence labeling, confocal microscopy, and 3D imaging, in order to understand anatomical and functional issues and to contribute to evolutionary questions. Although developmental studies on the gross morphology of bivalves have been extensively pursued, organogenesis including muscle development has been scarcely investigated so far. The present study describes in detail myogenesis in the scallop Nodipecten nodosus (Linnaeus, 1758) during larval and postmetamorphic stages by means of light, electron, and confocal microscopy. The veliger muscle system consists of an anterior adductor muscle, as well as four branched pairs of striated velum retractors and two pairs of striated ventral larval retractors. The pediveliger stage exhibits a considerably elaborated musculature comprising the velum retractors, the future adult foot retractor, mantle (pallial) muscles, and the anterior and posterior adductors, both composed of smooth and striated portions. During metamorphosis, all larval retractors together with the anterior adductor degenerate, resulting in the adult monomyarian condition, whereby the posterior adductor retains both myofiber types. Three muscle groups, i.e., the posterior adductor, foot retractor, and pallial muscles, have their origin prior to metamorphosis and are subsequently remodeled. Our data suggest a dimyarian condition (i.e., the presence of an anterior and a posterior adductor in the adult) as the basal condition for pectinids. Comparative analysis of myogenesis across Bivalvia strongly argues for ontogenetic and evolutionary independence of larval retractors from the adult musculature, as well as a complex set of larval retractor muscles in the last common bivalve ancestor.