Pteriomorph Bivalves Research Articles

A chromosome-level genome assembly of the disco clam, Ctenoides ales.

The bivalve subclass Pteriomorphia, which includes the economically important scallops, oysters, mussels, and ark clams, exhibits extreme ecological, morphological, and behavioral diversity. Among this diversity are five morphologically distinct eye types, making Pteriomorphia an excellent setting to explore the molecular basis for the evolution of novel traits. Of pteriomorphian bivalves, Limida is the only order lacking genomic resources, greatly limiting the potential phylogenomic analyses related to eyes and phototransduction. Here, we present a limid genome assembly, the disco clam, Ctenoides ales (C. ales), which is characterized by invaginated eyes, exceptionally long tentacles, and a flashing light display. This genome assembly was constructed with PacBio long reads and Dovetail Omni-CTM proximity-ligation sequencing. The final assembly is ∼2.3Gb and over 99% of the total length is contained in 18 pseudomolecule scaffolds. We annotated 41,064 protein coding genes and reported a BUSCO completeness of 91.9% for metazoa_obd10. Additionally, we report a complete and annotated mitochondrial genome, which also had been lacking from Limida. The ∼20Kb mitogenome has 12 protein coding genes, 22 tRNAs, 2 rRNA genes, and a 1,589 bp duplicated sequence containing the origin of replication. The C. ales nuclear genome size is substantially larger than other pteriomorphian genomes, mainly accounted for by transposable element sequences. We inventoried the genome for opsins, the signaling proteins that initiate phototransduction, and found that, unlike its closest eyed-relatives, the scallops, C. ales lacks duplication of the rhabdomeric Gq-protein-coupled opsin that is typically used for invertebrate vision. In fact, C. ales has uncharacteristically few opsins relative to the other pteriomorphian families, all of which have unique expansions of xenopsins, a recently discovered opsin subfamily. This chromosome-level assembly, along with the mitogenome, is a valuable resource for comparative genomics and phylogenetics in bivalves and particularly for the understudied but charismatic limids.

Opsin expression varies across larval development and taxa in pteriomorphian bivalves.

Many marine organisms have a biphasic life cycle that transitions between a swimming larva with a more sedentary adult form. At the end of the first phase, larvae must identify suitable sites to settle and undergo a dramatic morphological change. Environmental factors, including photic and chemical cues, appear to influence settlement, but the sensory receptors involved are largely unknown. We targeted the protein receptor, opsin, which belongs to large superfamily of transmembrane receptors that detects environmental stimuli, hormones, and neurotransmitters. While opsins are well-known for light-sensing, including vision, a growing number of studies have demonstrated light-independent functions. We therefore examined opsin expression in the Pteriomorphia, a large, diverse clade of marine bivalves, that includes commercially important species, such as oysters, mussels, and scallops. Genomic annotations combined with phylogenetic analysis show great variation of opsin abundance among pteriomorphian bivalves, including surprisingly high genomic abundance in many species that are eyeless as adults, such as mussels. Therefore, we investigated the diversity of opsin expression from the perspective of larval development. We collected opsin gene expression in four families of Pteriomorphia, across three distinct larval stages, i.e., trochophore, veliger, and pediveliger, and compared those to adult tissues. We found larvae express all opsin types in these bivalves, but opsin expression patterns are largely species-specific across development. Few opsins are expressed in the adult mantle, but many are highly expressed in adult eyes. Intriguingly, opsin genes such as retinochrome, xenopsins, and Go-opsins have higher levels of expression in the later larval stages when substrates for settlement are being tested, such as the pediveliger. Investigating opsin gene expression during larval development provides crucial insights into their intricate interactions with the surroundings, which may shed light on how opsin receptors of these organisms respond to various environmental cues that play a pivotal role in their settlement process.

Paleogene marine bivalves of the deep-water Keasey Formation in Oregon, Part II: The pteriomorphs

Systematic documentation of pteriomorph bivalves of the late Eocene–early Oligocene Keasey Formation in western Oregon follows previous monographic treatments of the anomalodesmatans and heteroconchs. It includes material from coeval Cascadia Margin strata in southwestern Washington in the context of major molluscan faunal turnover during the dramatic doubthouse climate transition from an ice-free tropical marine environment to the establishment of permanent polar ice caps and a cold temperate marine climate. The families represented are Crenellidae, Parallelodontidae, Glycymerididae, Limopsidae, Isognomonidae, Pectinidae, Propeamussiidae, and Limidae. New taxa include the genus Bathyisognomon and five new species: Limopsis squiresi, Bathyisognomon smithwickensis, Delectopecten kieli, Delectopecten keaseyorum, and Propeamussium (Parvamussium) mistensis. Small to minute mud pectens and glass scallops are among the most abundant and frequent taxa in the Keasey fauna, although they are poorly preserved and have been overlooked heretofore. Pteriomorphs are prominent elements of recurring associations of species in mudstone and fine-grained siltstone facies adjacent to three Keasey cold methane seeps. Previously described Keasey anomalodesmatans and heteroconchs in these seep-adjacent strata have living relatives adapted to dysoxia and toxic geochemistry. Because the unique macrofaunal associations in these settings are neither seep fauna nor part of the background fauna, this paper introduces and defines the concept of a transitional peri-seep biotope. Relationships, monophyly, systematic resolution within major pteriomorph groups, and global biogeographic distributions are reviewed in each systematic treatment. Recurring patterns include occurrences in active margin settings, inferred oscillatory deepening of the calcium carbonate compensation depth, late Eocene origin of two-layered oceans following establishment of the Antarctic Circumpolar Current, and biogeographic gateway changes that disrupted earlier Paleogene larval dispersal patterns.

Imbricated shell sculpture in benthic bivalves.

Molluscan shells display a high diversity of external sculpture. Sculptural elements may be symmetrical, where both edges of an element are morphologically similar, or asymmetrical, where one edge is steeper than the other. Asymmetrical sculpture can be ratcheted, with the leading edges (those in the direction of locomotion or growth) less steep than the trailing edges, or imbricated (leading edges steeper than trailing edges). While the ratcheted sculpture is better known, the diversity of imbricated sculpture has remained largely unexplored. In a survey of extant benthic shell-bearing molluscs, we document imbricated sculpture primarily in epifaunal bivalves or on the exposed sectors of shells of semi-infaunal bivalves. Imbricated sculpture is particularly widespread in pteriomorphian bivalves, but it is absent in the subclade Mytiloidea as well as in highly mobile Pectinidae. It also occurs in many carditid bivalves (Archiheterodonta) and in phylogenetically scattered euheterodonts. In several infaunal bivalves including species of Cardites (Carditidae), Hecuba (Donacidae), and Chione (Veneridae), comarginal elements on the posterior sector are imbricated whereas anterior comarginal ridges are ratcheted. Imbricated sculpture in bivalves tends to be concentrated on the upper (left) valves of pectinids or on the posterior sector of both valves in archiheterodonts and euheterodonts. Imbricated sculpture is uncommon in gastropods, even in epifaunal species, but does occur in the collabral ridges in some Vasidae and a few other groups. Expression of imbricated sculpture does not depend on shell mineral composition or microstructure. The ecological distribution and within-shell pattern of expression of imbricated sculpture point to the likelihood that this type of asymmetrical sculpture is both widespread and potentially functional. Additionally, we present a potential methodology whereby shell sculpture categories (symmetrical, ratcheted, and imbricated) may be quantified by comparing the lengths of corresponding leading and trailing edges across the shell surface.

Pliocene bivalves (Pteriomorphia) of Algiers Sahel (Algeria): Systematics and palaeoecology.

A hundred specimens of pteriomorph bivalves were collected from the marine deposits of the marly-sandy formations of Algiers Sahel, which correspond to transitional facies between the Piacenzian deep marly deposits and the Astian molassic deposits. They are herein analysed from a systematic, taphonomic, palaeoecological and paleoenvironmental point of view. The preliminary inventory list consists of 27 species belonging to eight families: Arcidae, Nuculidae, Glycymeridae, Spondylidae, Pectinidae, Plicatulidae, Gryphaeidae, and Ostreidae. Two sedimentary units with different bivalve biodiversity are recognized: the first: a shallow infralittoral unit characterised by large Flabellipecten alessii, Aequipecten angelonii, Ostrea lamellosa and O. edulis; the second: A deeper unit of circalittoral environment mainly includes Amusium cristatum. These bivalve shells display sclerobiont traces. Bioerosion traces are mostly assignable to clionid sponges (Entobia isp.), polychaete worms (Maeandropolydora isp. and Caulostrepsis isp.), bivalves (Gastrochaenolites isp.) and predatory gastropods (Oichnus isp.). Identified encrusting organisms are juvenile oyster shells, cirripedes, polychaete worms (serpulids), and indeterminate bryozoans. Analysis of boring and encrusting traces indicate a progressive environmental change from a relative high energy setting to a lower energy and deeper water setting, and correspond to a shallow sea with well-oxygenated waters.

Evolution of nacre- and prisms-related shell matrix proteins in the pen shell, Atrina pectinata

The molluscan shell is a good model for understanding the mechanisms underlying biomineralization. It is composed of calcium carbonate crystals and many types of organic molecules, such as the matrix proteins, polysaccharides, and lipids. The pen shell Atrina pectinata (Pterioida, Pinnidae) has two shell microstructures: an outer prismatic layer and an inner nacreous layer. Similar microstructures are well known in pearl oysters (Pteriidae), such as Pinctada fucata, and many kinds of shell matrix proteins (SMPs) have been identified from their shells. However, the members of SMPs that consist of the nacreous and prismatic layers of Pinnidae bivalves remain unclear. In this study, we identified 114 SMPs in the nacreous and prismatic layers of A. pectinata, of which only seven were found in both microstructures. 54 of them were found to bind calcium carbonate. Comparative analysis of nine molluscan shell proteomes showed that 69 of 114 SMPs of A. pectinata were found to have sequential similarity with at least one or more SMPs of other molluscan species. For instance, nacrein, tyrosinase, Pif/BMSP-like, chitinase (CN), chitin-binding proteins, CD109, and Kunitz-type serine proteinase inhibitors are widely shared among bivalves and gastropods. Our results provide new insights for understanding the complex evolution of SMPs related to nacreous and prismatic layer formation in the pteriomorph bivalves.

Phylogenetic comparisons reveal mosaic histories of larval and adult shell matrix protein deployment in pteriomorph bivalves

Molluscan shells are organo-mineral composites, in which the dominant calcium carbonate is intimately associated with an organic matrix comprised mainly of proteins and polysaccharides. However, whether the various shell matrix proteins (SMPs) date to the origin of hard skeletons in the Cambrian, or whether they represent later deployment through adaptive evolution, is still debated. In order to address this issue and to better understand the origins and evolution of biomineralization, phylogenetic analyses have been performed on the three SMP families, Von Willebrand factor type A (VWA) and chitin-binding domain-containing protein (VWA-CB dcp), chitobiase, and carbonic anhydrase (CA), which exist in both larval and adult shell proteomes in the bivalves, Crassostrea gigas and Pinctada fucata. In VWA-CB dcp and chitobiase, paralogs for larval and adult SMPs evolved before the divergence of these species. CA-SMPs have been taken as evidence for ancient origins of SMPs by their presumed indispensable function in biomineralization and ubiquitous distribution in molluscs. However, our results indicate gene duplications that gave rise to separate deployments as larval and adult CA-SMPs occurred independently in each lineage after their divergence, which is considerably more recent than hitherto assumed, supporting the “recent heritage and fast evolution” scenario for SMP evolution.

Hard to get, easy to lose: Evolution of mantle photoreceptor organs in bivalves (Bivalvia, Pteriomorphia).

Morphologically diverse eyes have evolved numerous times, yet little is known about how eye gain and loss is related to photic environment. The pteriomorphian bivalves (e.g., oysters, scallops, and ark clams), with a remarkable range of photoreceptor organs and ecologies, are a suitable system to investigate the association between eye evolution and ecological shifts. The present phylogenetic framework was based on amino acid sequences from transcriptome datasets and nucleotide sequences of five additional genes. In total, 197 species comprising 22 families from all five pteriomorphian orders were examined, representing the greatest taxonomic sampling to date. Morphological data were acquired for 162 species and lifestyles were compiled from the literature for all 197 species. Photoreceptor organs occur in 11 families and have arisen exclusively in epifaunal lineages, that is, living above the substrate, at least five times independently. Models for trait evolution consistently recovered higher rates of loss over gain. Transitions to crevice-dwelling habit appear associated with convergent gains of eyespots in epifaunal lineages. Once photoreceptor organs have arisen, multiple losses occurred in lineages that shift to burrowing lifestyles and deep-sea habitats. The observed patterns suggest that eye evolution in pteriomorphians might have evolved in association with light-guided behaviors, such as phototaxis, body posture, and alarm responses.

Short-lived “Bakevelliid-Sea” in the Aptian Romualdo Formation, Araripe Basin, northeastern Brazil

New Aptian (Lower Cretaceous) bakevelliid bivalves are described for the Romualdo Formation, Santana Group, Araripe Basin, northeastern Brazil. Together with the other known member of the family Bakevelliidae, already recorded from the unit (i.e., Aguileria dissita), the new bivalves (Araripevellia musculosa gen. et sp. nov., Aguileria romualdoensis sp. nov., and Gen. et sp. indet.) indicate that the Romualdo bakevelliid fauna was more diverse than previously realized. Bakevelliid-rich carbonates, some with specimens preserved in situ, are restricted to the upper third of this unit, a stratigraphic interval yielding also echinoderm-, gastropod- and stromatolite-bearing limestones. These pteriomorphian bivalves were widely distributed in the Romualdo Formation and are a testimony of the short-lived Bakevelliid-Sea that flooded the whole Araripe Basin during the Aptian. Notably, Aguileria romualdoensis sp. nov. closely resembles Aguileriarenauxiana from the Cenomanian Woodbine Formation, Texas, US. In addition, Aguileria dissita is also recorded in the upper Aptian–Albian Riachuelo Formation of the Sergipe-Alagoas Basin. Together with other macroinvertebrates (i.e., gastropods, echinoderms, bivalves) the bakevelliid fauna of the Romualdo Formation can be tightly correlated with that of the Riachuelo Formation, supporting a paleogeographic scenario with a marine ingression flooding the Araripe Basin from the southeast, probably via the seaway developed in the Recôncavo-Tucano basin area. Finally, sedimentologic, stratigraphic and paleontological data indicates that the fate of the bakevelliids in the Romualdo Formation was linked to the onset of continentalization of the Araripe Basin.

Silurian and Devonian Pteriomorph Bivalves from Bolivia

Pteriomorph bivalves from the Silurian and the Devonian beds of Central Andes Basin of Western Gondwana are herein presented. They were collected in ten scattered outcrops in Eastern Cordillera, South of Western Altiplano, South of Interandean and Subandean Bolivia. A total of 54 specimens of a good to regular state of preservation were studied. It is the first time that genera Leptodesma (Leptodesma), Ptychopteria (Ptychopteria) and Ptychopteria (Actinopteria) are reported from Ludlowian beds of the Central Andes Basin: Leptodesma (Leptodesma) sp. B from Corregidores and Huari, Ptychopteria (Ptychopteria) sp. B from Chaquimayu and Ptychopteria (Actinopteria) cf. migrans migrans from Tarabuco and Alarache. A very small Ptychopteria (Actinopteria) sp. is reported from Ludlowian of Tarabuco and from early Lochkovian of Corregidores. It is the first time that Pragian–Emsian pteriomorphs as Ptychopteria (Ptychopteria) sp. A from Sella, and Leptodesma (Leptodesma) sp. A from Huacareta are described. It is also the first time that Eifelian pteriomorphs as Ptychopteria (Actinopteria) eschwegii and Leptodesma (Leptodesma) sp. A from La Escalera and Tiraque-Limbo are documented. This research contributes to the as yet inaccurately known Silurian and Devonian palaeogeography of the Central Andes Basin and is an update of old systematic descriptions of few Pteriomorph bivalves from late 19th and early 20th centuries.

Form and function of tentacles in pteriomorphian bivalves.

Tentacles are remarkable anatomical structures in invertebrates for their diversity of form and function. In bivalves, tentacular organs are commonly associated with protective, secretory, and sensory roles. However, anatomical details are available for only a few species, rendering the diversity and evolution of bivalve tentacles still obscure. In Pteriomorphia, a clade including oysters, scallops, pearl oysters, and relatives, tentacles are abundant and diverse. We investigated tentacle anatomy in the group to understand variation, infer functions, and investigate patterns in tentacle diversity. Six species from four pteriomorphian families (Ostreidae, Pinnidae, Pteriidae, and Spondylidae) were collected and thoroughly investigated with integrative microscopy techniques, including histology, scanning electron microscopy, and confocal microscopy. Tentacles can be classified as middle fold tentacles (MFT) and inner fold tentacles (IFT) according to their position with respect to the folds of the mantle margin. While MFT morphology indicates intense secretion of mucosubstances, no evidence for secretory activity was found for IFT. However, both tentacle types have appropriate ciliary distribution and length to promote mucus transportation for cleaning and lubrication. Protective and sensory functions are discussed based on different lines of evidence, including secretion, cilia distribution, musculature, and innervation. Our results support the homology of MFT and IFT only for Pterioidea and Ostreoidea, considering their morphology, the presence of ciliated receptors at the tips, and branched innervation pattern. This is in accordance with recent phylogenetic hypotheses that support the close relationship between these superfamilies. In contrast, major structural differences indicate that MFT and IFT are probably not homologous across all pteriomorphians. By applying integrative microscopy, we were able to reveal anatomical elements that are essential for the understanding of homology and function when dealing with such superficially similar structures.

Abyssal fauna of the UK-1 polymetallic nodule exploration area, Clarion-Clipperton Zone, central Pacific Ocean: Mollusca.

We present the first DNA taxonomy publication on abyssal Mollusca from the Clarion-Clipperton Zone (CCZ), central Pacific ocean, using material collected as part of the Abyssal Baseline (ABYSSLINE) environmental survey cruise ‘AB01’ to the UK Seabed Resources Ltd (UKSRL) polymetallic-nodule exploration area ‘UK-1’ in the eastern CCZ. This is the third paper in a series to provide regional taxonomic data for a region that is undergoing intense deep-sea mineral exploration for high-grade polymetallic nodules.Taxonomic data are presented for 21 species from 42 records identified by a combination of morphological and genetic data, including molecular phylogenetic analyses. These included 3 heterodont bivalves, 5 protobranch bivalves, 4 pteriomorph bivalves, 1 caudofoveate, 1 monoplacophoran, 1 polyplacophoran, 4 scaphopods and 2 solenogastres. Gastropoda were recovered but will be the subject of a future study. Seven taxa matched published morphological descriptions for species with deep Pacific type localities, and our sequences provide the first genetic data for these taxa. One taxon morphologically matched a known cosmopolitan species but with a type locality in a different ocean basin and was assigned the open nomenclature ‘cf’ as a precautionary approach in taxon assignments to avoid over-estimating species ranges. One taxon is here described as a new species, Ledella knudseni sp. n. For the remaining 12 taxa, we have determined them to be potentially new species, for which we make the raw data, imagery and vouchers available for future taxonomic study. The Clarion-Clipperton Zone is a region undergoing intense exploration for potential deep-sea mineral extraction. We present these data to facilitate future taxonomic and environmental impact study by making both data and voucher materials available through curated and accessible biological collections.

Physical versus Biological Control in Bivalve Calcite Prisms: Comparison of Euheterodonts and Pteriomorphs.

Multiple groups of bivalve molluscs produce calcitic shell layers, many of these broadly classified as "prismatic." Various pteriomorphian bivalves (such as oysters, pterioids, and mussels) secrete prismatic microstructures with high organic content and clear, strong biological control. However, we present the results of a detailed analysis by scanning electron microscopy (SEM), thermogravimetric analysis, and electron backscatter diffraction to characterize the calcitic prisms in two different clades within the euheterodont bivalves: the extant Chama arcana and the extinct rudists. These results show that the form of prisms constructed is both closely similar between the two taxa and significantly different from those of the pteriomorph bivalves. Most notably, C. arcana and the extinct rudists lack the clear organic outer envelopes and uniform polygonal, cross-sectional appearance. Instead, they form interdigitating crystals of very varied diameters, with some crystals encapsulating others. We advocate retaining the term "fibrillar prisms" to classify these euheterodont microstructures. These fibrillar prisms are more closely similar to abiotic speleothem deposits than to the calcitic prisms of pteriomorph bivalves. We argue that calcite prism growth in euheterodonts is dominated by abiotic constraints whereas, in pteriomorphs (such as oysters, pterioids, and mussels), it is under strong biological control.

On the Evolutionary Significance of the Mantle Margin in Pteriomorphian Bivalves

The bivalve mantle margin comprises the free portion of the pallial lobes, and often bears muscular, sensory or secretory structures located on extensions of the mantle, called mantle folds. In the bivalve Infraclass Pteriomorphia, which underwent an extensive adaptive radiation in epifaunal habitats, the mantle margin exhibits an enormous diversity in mantle fold organization and associated structures. The present work reviews the current knowledge of the mantle margin in Pteriomorphia and discusses how the mantle margin can be used as a model for investigating the evolution of the marine epifaunal benthos as many species in this community have undergone similar selective pressures and developed comparable morphological adaptations, such as ciliated tentacular organs. Herein, we stress how additional investigations are necessary to cover the huge diversity seen in this taxonomic group. Given the scarcity of broad comparative studies of bivalves, including Pteriomorphia, the homology of their pallial features is still not clear. Moreover, although it is suspected that mantle margin diversification is correlated with transitions in pteriomorphian life habits, no hypotheses have been tested within a phylogenetic framework. To address these questions requires extensive comparative analyses of mantle margin diversity in Pteriomorphia that focuses on: 1) genetic expression and molecular dynamics in the mantle margin; 2) mantle margin morphogenesis, 3) assessment and test of hypotheses on homology, convergent and parallel evolution of mantle margin characters, and 4) testing possible correlations between mantle margin morphological diversity and lifestyle transitions. In a broader sense, by using Pteriomorphia as a model clade, we will gain insight into the macroecology of the marine epifauna.

Identification of genes associated with shell color in the black-lipped pearl oyster, Pinctada margaritifera.

BackgroundColor polymorphism in the nacre of pteriomorphian bivalves is of great interest for the pearl culture industry. The nacreous layer of the Polynesian black-lipped pearl oyster Pinctada margaritifera exhibits a large array of color variation among individuals including reflections of blue, green, yellow and pink in all possible gradients. Although the heritability of nacre color variation patterns has been demonstrated by experimental crossing, little is known about the genes involved in these patterns. In this study, we identify a set of genes differentially expressed among extreme color phenotypes of P. margaritifera using a suppressive and subtractive hybridization (SSH) method comparing black phenotypes with full and half albino individuals.ResultsOut of the 358 and 346 expressed sequence tags (ESTs) obtained by conducting two SSH libraries respectively, the expression patterns of 37 genes were tested with a real-time quantitative PCR (RT-qPCR) approach by pooling five individuals of each phenotype. The expression of 11 genes was subsequently estimated for each individual in order to detect inter-individual variation. Our results suggest that the color of the nacre is partially under the influence of genes involved in the biomineralization of the calcitic layer. A few genes involved in the formation of the aragonite tablets of the nacre layer and in the biosynthesis chain of melanin also showed differential expression patterns. Finally, high variability in gene expression levels were observed within the black phenotypes.ConclusionsOur results revealed that three main genetic processes were involved in color polymorphisms: the biomineralization of the nacreous and calcitic layers and the synthesis of pigments such as melanin, suggesting that color polymorphism takes place at different levels in the shell structure. The high variability of gene expression found within black phenotypes suggests that the present work should serve as a basis for future studies exploring more thoroughly the expression patterns of candidate genes within black phenotypes with different dominant iridescent colors.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1776-x) contains supplementary material, which is available to authorized users.

Molluscan assemblages under the influence of peat-draining rivers off East Sumatra, Indonesia

The central Indo-west Pacific biodiversity hotspot is of outstanding biological interest in terms of both taxonomy and ecology. However, the molluscan fauna of the region is poorly known. Here we present death assemblages of the subtidal (1–56 m) waters off Eastern Sumatra, Indonesia. Molluscan shells were sampled from a variety of settings from estuaries to coral reef-related carbonate environments. A total of 5064 shells was counted and 197 species were identified. Four shelly death assemblages which are defined by characteristic taxa are found in specific environments. A deposit-feeding community with low diversity and low abundances was recorded in settings with high amounts of terrigenous mud. Greater abundances and higher diversity were found farther offshore, especially in carbonate sediments in the vicinity of offshore islands where pteriomorphian bivalves are characteristic taxa. Protobranch bivalves, especially a species of Nuculana, appear to be best adapted to the organic-rich but food-limited, muddy substrate of the proximal marine environment influenced by peat-draining rivers. Thus, in addition to dominating deep-sea molluscan assemblages, some protobranch bivalves appear to be specialists in exploiting refractory organic materials of shelf environments.

Rhogocytes in gastropod larvae: developmental transformation from protonephridial terminal cells

AbstractRhogocytes, terminal cells of protonephridia, and podocytes of metanephridial systems share an architectural feature that creates an apparent sieving device. The sieve serves to ultrafilter body fluid during the excretion and osmoregulation process carried out by nephridial systems, but its function in rhogocytes is unclear. Rhogocytes are molluscan hemocoelic cells that appear to have various functions related to metabolism of metal ions, including synthesis of hemocyanin in some gastropods and metal detoxification in pteriomorph bivalves. A hypothesis that proposed developmental and possibly evolutionary conversion between protonephridial terminal cells and rhogocytes has never been further explored; indeed, information on the occurrence of rhogocytes in molluscan developmental stages is meager. We used transmission electron microscopy to show that rhogocytes are present within larvae of eight species of gastropods sampled from the three major gastropod clades with a feeding larval stage in the life history. In larvae of a heterobranch gastropod, a rhogocyte was located next to each terminal cell of a pair of protonephridia that flanked the foregut, whereas all six species of caenogastropod larvae and a neritimorph larva that we examined had rhogocytes, but no protonephridia, in this location. We did not find ring‐shaped profiles of hemocyanin decamers within rhogocytes of larvae or pre‐hatch embryos. Rhogocytes in newly released larvae of Nerita melanotragus contained orderly bundles of cylinders, but the diameter of the cylinders was only 70% of the diameter typical of hemocyanin multidecamers. By examining embryos of the caenogastropod Nassarius mendicus at four successive developmental time points that bracketed the occurrence of larval hatching, we found that terminal cells from non‐functional protonephridia in pre‐hatch embryos transformed into rhogocytes around the time of hatching. This empirical evidence of ontogenetic transformation of protonephridial terminal cells into rhogocytes might be interpreted as developmental recapitulation of an evolutionary transition that occurred early in molluscan history.

Comparison of oxygen consumption byTerebratalia transversa(Brachiopoda) and two species of pteriomorph bivalve molluscs: implications for surviving mass extinctions

The Permian/Triassic mass extinction marks a permanent phylogenetic shift in the composition of the sessile benthos, from one largely dominated by articulate brachiopods to one dominated by mollusks. Widespread evidence of oceanic hypoxia and anoxia at this time provides a possible selective kill mechanism that could help explain the large taxonomic losses in brachiopods compared to the morphologically and ecologically similar bivalve molluscs. Our study compared the oxygen consumption of an articulate brachiopod,Terebratalia transversa, with that of two pteriomorph bivalves,Glycymeris septentrionalisandMytilus trossulus, under normoxia and hypoxia, as well as their tolerance to anoxia, to gain insight into the relative metabolic characteristics of each group. We found no significant difference in the oxygen consumption of the three species when normalized to the same dry-tissue mass. However, when calculated for animals of the same external linear dimensions, bivalve oxygen consumption was two to three times greater than that of brachiopods. Our results also showed no significant decrease in the oxygen consumption of the three species until measured at a partial pressure of oxygen ∼10% of normoxic values. Finally,T. transversaandM. trossulusshowed no significant difference in their tolerance to complete anoxia, but both showed a much lower tolerance than another bivalve,Acila castrensis. Findings from this study suggest that oxygen limitation is unlikely to account for the observed selective extinction of brachiopods during the Permian/Triassic mass extinction. Results may provide valuable information for assessing hypotheses put forth to explain why articulate brachiopods continue to remain a relatively minor group in marine environments.

Crystallographic reorganization of the calcitic prismatic layer of oysters

The calcitic columnar prisms of pteriomorphian bivalves have the crystallographic c-axis oriented perpendicular to the shell surface and the a-axes rotated without any preferential orientation. In oysters, SEM, XRD and EBSD analyses show that individual prisms initially have their a-axes randomly oriented but are able to progressively orient them parallel to those of their neighbors. This ability is apparently confined to groups, such as oysters and scallops, in which prisms are internally constituted by smaller lath-like crystal units. We have developed a competition model - not between prisms, but between the lath-like secondary units of prisms - which is based on differences in the inclination of laths relative to the shell growth surface. Units having a growth component which coincides with the growth direction protrude faster from the growth surface and out-compete those which are not favorably oriented, which reduces the overall dispersion of the a-axes of the prismatic lamella. The extent of re-alignment increases with the relative inclination of the growth surface and the length attained by the prisms. Oysters are the only group in which these two characters are pronounced enough to provide a measurable re-alignment. The proposed competition model is unprecedented in biomaterials and reveals how important crystal growth processes are in microstructure organization.

Brachiopods from cryptic coral reef habitats in the northern Red Sea

In contrast to the Palaeozoic to Jurassic fossil record, modern tropical and subtropical shallow-water brachiopods are typically small-sized and mostly restricted to cryptic habitats in coral reefs, but information on microhabitat-composition is scant. At Dahab, northern Red Sea, living brachiopods of the genus Argyrotheca were only detected on massively encrusted coral colonies attached to encrusting foraminifers and coralline red algae. Three samples from autochthonous sediments underneath coral colonies are comparatively rich in the brachiopod genera Megerlia and Argyrotheca, and additionally show low numbers of Novocrania and Thecidellina. Based on a coarse-grain analysis including more than 16,000 components >1 mm, these brachiopod shells co-occur with skeletal components of 11 higher taxa. Decapods, fixosessile foraminifers, molluscs, scleractinians, and coralline red algae clearly dominate the assemblages. Brachiopods in this study always contribute less than 2% to the sediment composition. This confirms previous results that even in brachiopod habitats the contribution of brachiopod shells to the total sediment composition is almost negligible. Our study indicates that brachiopods co-occur with pteriomorph bivalves and other epifauna in the cryptic habitats with limited space for encrusters or epibionts on the undersides of scleractinians and it tentatively supports the hypothesis of brachiopods preferring habitats with low grazing pressure, because shelly components of grazers (polyplacophorans and regular echinoids) are rare in our samples.