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Progression of internalization of the ligament and consequent loss of posterior hinge teeth in Nucinellidae. A. Nucinella dalli. B. N. boucheti (after La Perna, 2005). C. N. serrei Lamy. D. Huxleyia habooba n. sp. E. H. concentrica. A, C-E in NMW. Not to scale.
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Nucinellidae are a family of small, monomyarian, nuculoid marine bivalves that live at depths from 6–3,500 m. Related to the Solemyidae, they are suspected of chemosymbiosis with sulphur-oxidizing bacteria, but hitherto without morphological or molecular confirmation. Two new species, Nucinella owenensis and Huxleyia habooba, were collected at dept...
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... ligament has always been stated to be opisthodetic and is generally so, but in some minute species it is amphi- detic lying immediately below the beaks (see N. dalli, Fig. 7). The ligament is either external, or in a sunken resi- lifer as in Nucinella, or wholly internal as in Huxleyia. In species with a sunken or internal ligament there is variation in the extent to which the ligament impacts the posterior teeth (Fig. 7). This observation renders the family Huxleyiidae unwarranted and also brings into ...
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... so, but in some minute species it is amphi- detic lying immediately below the beaks (see N. dalli, Fig. 7). The ligament is either external, or in a sunken resi- lifer as in Nucinella, or wholly internal as in Huxleyia. In species with a sunken or internal ligament there is variation in the extent to which the ligament impacts the posterior teeth (Fig. 7). This observation renders the family Huxleyiidae unwarranted and also brings into question the current generic definitions; resolution of this is beyond the scope of this ...
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Site 723 is located in a water depth of 808 m at the center of the oxygen minimum zone and the middle part of the main thermocline on the Oman Margin. Oxygen isotope curves of planktonic δ18OP and benthic δ18OB can be traced back continuously to Stage 23 with high resolution measurements. A tentative correlation to Stage 53 has been tried using oxy...
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... Members of the class Bivalvia have acquired chemosynthetic symbiosis multiple times, with eight families (i.e. Basterotiidae, Nucinellidae, Lucinidae, Mytilidae, Solemyidae, Teredinidae, Thyasiridae and Vesicomyidae) having been reported to host methanotrophic and/or thioautotrophic bacteria (Ip et al., 2021;Oliver & Taylor, 2012;Sun et al., 2017). Among them, mytilid mussels, lucinid clams and vesicomyid clams have been extensively studied concerning symbiont chemoautotrophic capacity (Petersen et al., 2016), molecular cross-talk between symbiont and host (Ip et al., 2021;Sun et al., 2017), mode of symbiont transition (Ikuta et al., 2016) and symbiont strain diversity (Ansorge et al., 2019) but to appreciate the diversity of symbiosis in Bivalvia and to understand their evolution, it is urgent to study the symbiosis in the other families of symbiotic bivalves. ...
Previous studies have deciphered the genomic basis of host-symbiont metabolic complementarity in vestimentiferans, bathymodioline mussels, vesicomyid clams and Alviniconcha snails, yet little is known about the chemosynthetic symbiosis in Thyasiridae-a family of Bivalvia regarded as an excellent model in chemosymbiosis research due to their wide distribution in both deep-sea and shallow-water habitats. We report the first circular thyasirid symbiont genome, named Candidatus Ruthturnera sp. Tsphm01, with a size of 1.53 Mb, 1521 coding genes and 100% completeness. Compared to its free-living relatives, Ca. Ruthturnera sp. Tsphm01 genome is reduced, lacking components for chemotaxis, citric acid cycle and de novo biosynthesis of small molecules (e.g. amino acids and cofactors), indicating it is likely an obligate intracellular symbiont. Nevertheless, the symbiont retains complete genomic components of sulphur oxidation and assimilation of inorganic carbon, and these systems were highly and actively expressed. Moreover, the symbiont appears well-adapted to anoxic environment, including capable of anaerobic respiration (i.e. reductions of DMSO and nitrate) and possession of a low oxygen-adapted type of cytochrome c oxidase. Analysis of the host transcriptome revealed its metabolic complementarity to the incomplete metabolic pathways of the symbiont and the acquisition of nutrients from the symbiont via phagocytosis and exosome. By providing the first complete genome of reduced size in a thyasirid symbiont, this study enhances our understanding of the diversity of symbiosis that has enabled bivalves to thrive in chemosynthetic habitats. The resources will be widely used in phylogenetic, geographic and evolutionary studies of chemosynthetic bacteria and bivalves.
... Chemosymbiosis is well documented in many bivalve groups (see Taylor and Glover (2010) for review). The bivalve families that contain chemosymbiotic taxa are Lucinidae, Thyasiridae, Solemyidae, Vesicomyidae, Teredinidae, and Mytilidae (there is circumstantial evidence for chemosymbiosis in several members of Nucinellidae and at least one species in the bivalve family Basterotiidae, though nutritional chemoautotrophy has not yet been demonstrated; Oliver and Taylor 2012;Oliver, 2013). Most recorded bivalve chemosymbionts belong to Gammaproteobacteria (Sogin et al., 2021), however the nature of symbioses varies considerably in metabolism, transmission modes, and hostsymbiont nutrient exchange. ...
... The Nucinellidae are another bivalve family in the order Solemyida with taxa found in a range of marine habitats, including deep sea sediments and tropical seagrass beds (Glover and Taylor, 2013). Chemosymbiosis has been inferred in this group as some nucinellids have a reduced or absent gut (Kuznetsov, 1984) and bacteriocytes are present in the gill tissue of at least two species (Oliver and Taylor, 2012). However, empirical assessments of chemoautotrophic activity in these taxa are wanting. ...
Many bivalves and gastropods from marine reducing environments such as deep ocean hydrothermal vents and seeps host chemosynthetic bacteria in a nutritional symbiosis. Despite their functional similarities, the distribution of chemosymbiosis in these two mollusk classes is surprisingly uneven: the number of bivalve species known to host chemosynthetic symbionts is more than twenty times that of gastropods, and chemosymbiotic bivalves are reported from a far greater diversity of marine habitats. Here we explore the potential drivers for this trend, including but not limited to physiological differences, habitat characteristics, and sampling bias. Sampling bias likely contributes to the magnitude of the observed discrepancy, but we posit that the phenomenon itself reveals how intrinsic (e.g. morphology) and extrinsic (e.g. organic matter availability) factors might have shaped the distribution of extant gastropod and bivalve associations. These observations also serve as an impetus for increasing investigation into gastropods and other mollusks from chemically reducing environments to better understand the evolution and ecology of chemosymbiosis among molluscan hosts.
... This is particularly well supported for the solemyids of the Eifelian Hollard Mound, for which cooperation with chemosymbionts is suggested by their behaviour similar to their extant, chemosynthetic relatives . Accordingly, some morphological arguments imply that chemosymbiosis in Solemyidae dates back to the early Ordovician and may be as old as the family (Waller 1998;Cope 2000;Oliver and Taylor 2012). The two species of the modiomorphid genus Ataviaconcha, Ataviaconcha sp. from the Ludfordian El Borj site, and A. wendti from the Eifelian Hollard Mound share a suite of characteristic features, many observed also in modern seep-dwelling bivalves. ...
Despite much effort aimed to better constrain the fossil record of chemosynthesis-based communities, our understanding of their early evolution remains fragmentary. Until recently, a dominant perception was that, unlike the Cenozoic, bivalve-dominated chemosynthesis-based ecosystems, the Palaeozoic to mid-Mesozoic methane seeps and hydrothermal vents were dominated by brachiopods. Recent discoveries from the oldest-known seep palaeoecosystems, found in the middle Palaeozoic of Morocco, have questioned this view, documenting Silurian and Middle Devonian seeps with abundant large, semi-infaunal, modiomorphid bivalves. While representing a lineage unrelated to modern seep-obligate bivalves, the mid-Palaeozoic seep bivalves display morphology and occurrence mode strikingly similar to those of their modern counterparts, suggesting their chemosymbiotic lifestyle. The studies of Moroccan seeps provide, therefore, a new look at the concept of modern chemosynthesis-based communities as a ‘glimpse of antiquity’, showing that, despite the taxonomic differences, it is true in terms of recurring morphological themes. The presence of ‘modern-type’, bivalve-dominated seep communities in the Silurian and mid-Devonian of Morocco is particularly intriguing given the absence of rich bivalve clusters at younger Palaeozoic seeps, including the youngest, upper Devonian seep of Morocco, which hosts the oldest occurrence of dimerelloidean brachiopods, a lineage notably successful in seep assemblages until the Early Cretaceous.
... The genus Solemya is subdivided into the subgenera Solemya s.s.; Solemyarina Iredale, 1931;Petrasma Dall, 1908a;Zesolemya Iredale, 1939;Austrosolemya Taylor, Glover, and Williams, 2008;and Pseudacharax Huber, 2010, based on the difference in length and character of the anterior ligament extension, relation of the chondrophore to posterior adductor muscle scar, and presence of a buttress, supporting the anterior margin of posterior adductor muscle scar. A detailed discussion and table of the differences between particular subgenera of Solemya were presented by Taylor et al. (2008), Kamenev (2009), Oliver andTaylor (2012), and Hryniewicz et al. (2014). The Paleozoic genera Dystactella Hall andWhitfield, 1872, andClinopistha Meek andWorthen, 1870, have commarginal ornament and an external ligament. ...
... The family Nucinellidae Vokes, 1956, is considered either as the sister taxon to Solemyidae ( Fig. 10.4) or at least closely related to it (Sharma et al. 2013). The species of Nucinella are shallow burrowers and are not obligate vent and seep inhabitants but also occur in "normal" marine sediments of 6 m to 3500 m in depth (e.g., Matsukuma et al. 1982;La Perna 2005;McLeod et al. 2010;Oliver and Taylor, 2012). Chemosymbiosis has been suggested for some species of Nucinella based on their reduced or absent digestive tract (e.g., Kuznetsov and Shileyko 1984;Reid 1998). ...
... These suggestions were partially confirmed by the accumulation of light carbon in the tissues of Nucinella maoriana, similar in magnitude to that of species of Thyasiridae and Solemyidae with confirmed chemosymbiosis found in their immediate surroundings (McLeod et al. 2010). Oliver and Taylor (2012) found potentially chemoautotrophic bacteria in the gills of the modern species Nucinella owenensis and Huxleyia habooba, which were recovered from the oxygen-minimum zone in the Arabian Sea off of southern Oman. Thus, Nucinella potentially is a member of chemosynthetic communities in seep sites. ...
Bivalves are an important part of the methane seep fauna ever since seeps appeared in the geologic record. The chronostratigraphic ranges of seep-inhabiting chemosymbiotic bivalves show an overall increase in diversity at seeps since the Paleozoic. The most common group at Paleozoic and early Mesozoic seeps are modiomorphids, with a few additional records of solemyids and anomalodesmatans. The most common infaunal chemosymbiotic bivalve taxa at modern seeps, lucinids and thyasirids, appeared at seeps in the Late Jurassic and earliest Cretaceous. They diversified during the Cretaceous synchronous with the peak of the “Mesozoic Marine Revolution” and first occurrences of gastropod predatory drill holes in the shells of seep-inhabiting bivalves, soon after the appearance of these gastropods in the mid-Cretaceous. The two dominant bivalve clades of the modern vent and seep fauna, bathymodiolins and vesicomyids, appeared in the Eocene. Their origin has been linked to a deep-water extinction event at the Paleocene-Eocene Thermal Maximum. However, the fossil record of chemosymbiotic bivalves at seeps during this time interval does not display any extinction. Rather, the mid-Eocene appearance of semi-infaunal and epifaunal bivalves such as bathymodiolins and vesicomyids might be linked to a dramatic rise in seawater sulfate concentrations at this time.KeywordsBivalvesChemosymbiosisEvolutionSulfate concentrationMesozoic marine revolutionSolemyidaeNucinellidaeBathymodiolinaeModiomorphidaeKalenteridaeLucinidaeThyasiridaeVesicomyidaeAnomalodesmatas
... Little is presently known about protobranchs, a subclass of predominantly deep-sea bivalve mollusks possessing certain traits considered ancestral or primitive within bivalves (González et al., 2015). The presently existing orders of these bivalves include Nuculanida, Nuculida, and Solemyida (Mollusca: Bivalvia: Protobranchia), together comprising approximately 750 species (Zardus, 2002), most of which are deposit-feeders living in sediments, while some others host chemoautotrophic and sulfide-oxidizing bacteria (Oliver et al., 2011;Oliver & Taylor, 2012). ...
Understanding aspects of development in animals posessing certain ancestral traits can provide key insights into the evolution of various larval forms of invertebrates. Little is presently known concerning the neurodevelopment of Protobranchia, a group of bivalve mollusks. We are first to demonstrate that neurogenesis of the pericalymma larvae of the protobranch Acila insignis differs dramatically from that of the larval nervous system of autobranchia species as revealed by serotonin (5-HT) and FMRFamide antibodies and whole-mount confocal microscopy. Early in the development of pericalymma, two and then three flask-shaped cells immunopositive for 5-HT appear in the apical organ (AO). Later on, in mid-stage larvae, cells immunostained for FMRFamide appear in the dorsal portion of the larva, including a weak signal in the AO. Immediately prior to metamorphosis, the larval FMRFamide-ergic nervous system consists of a single cell in the AO together with several non-sensory cells in the posterior and dorsal regions. No neuronal connections between the larval neuronal cell groups were observed. However, despite the obvious differences in early neurogenesis, there are clear neuromorphological similarities of the studied protobranch species to (1) spiralians (by the presence of an AO), (2) certain trochozoans (by peripheral cells containing FMRFamide) and (3) bivalve mollusks (by AO including three flask-shaped cells revealed by immunostaining for 5-HT). Thus, the nervous system of A. insignis is similar to that of other mollusks and lophotrochozoans due to the presence of an AO, while differing from all the studied groups in other characters (location and composition of FMRFamide cells). Morphological and molecular development of key protobranch taxa need to be further studied in order to infer the evolution of mollusks.
... Mollusca não tem sido relatado como um grupo muito abundante nas regiões de talude e cânions, entretanto a família Nucinellidae apresentou altas abundâncias em ambos os cânions da bacia de Sergipe e sul de Alagoas. Os membros da família Nucinellidae, que foram muito abundantes nos cânions do São Francisco e Japaratuba, são relatados como associados com sedimentos ricos em matéria orgânica (Matsukuma et al., 1982;McLeod et al., 2010;Oliver;Taylor, 2012), em profundidades em torno de 400 a 500 metros nos fiordes do Indo-Pacífico (McLeod et al., 2010), mas na região dos cânions portugueses, os Aplacophora dominaram em abundância (Cunha et al., 2011). Vetter e Dayton (1998) Diversos trabalhos apontam que uma relação negativa entre densidade de organismos bentônicos e profundidade está relacionada à disponibilidade de matéria orgânica (Flach, 2002;Helder;Epping, 1999), mas não encontramos esta relação no presente trabalho. ...
The macrobenthic community from Sergipe-Alagoas Basin continental slope was sampled for the characterization of the composition and structure in relation to the temporal, bathymetric and latitudinal gradients. Therefore, samples were collected in 38 stations, 14 of which are located in the São Francisco and Japaratuba canyons, involving samples from 50 to 3000 m deep in the dry and rainy season of 2013. Sediment and deep water parameters were also sampled. The organisms were collected with a box-corer, each replica with an area of 0.09 m2, fixed in 10 % formaldehyde, washed in fresh water through 300 mm mesh sieves and preserved in 70 % alcohol. A total of 94.274 individuals were recorded and distributed in 11 phyla and 197 families. Polychaeta dominated in density (49 %) and Crustacea in richness (44.3 %), when considered at family level. 39 % of the families were considered rare because they occurred in less than three stations and 24 % as frequent because they occurred in more than 20 stations. The community structure analysis showed absence of a temporal component, a strong bathymetric factor and a greater richness and abundance in the canyons when compared to other transects of the continental slope. The environmental variables that best explained the spatial distribution patterns of the composition and abundance of the analyzed families were depth, temperature, salinity, total organic carbon, total carbonate, organic phosphorus and total silt, accounting for 38.4 % of the variability found.
... The Nuculida and Nuculanida are generally deposit feeders (Stanley, 1970;Zardus, 2002). The Solemyida host chemoautotrophic bacteria within their gills (Distel, 1998;Stewart & Cavanaugh, 2006); the origin of their chemosymbiosis-based lifestyle is estimated to date back to the early Ordovician (Oliver & Taylor, 2012). Protobranchs have changed little in their morphologies and habitats (Allen, 1983) and remained important components of marine soft-sediment assemblages over time (Rhoads & Young, 1970). ...
... The present phylogeny is also concordant with the fossil record in recovering the clade Solemyoidea + Manzanelloidea as the order Solemyida (Cope, 2000;Pojeta, 1988). A number of shared anatomical traits (Allen & Sanders, 1969) as well as chemosymbiotic lifestyles (Oliver & Taylor, 2012) further support the close relationship of the two superfamilies. ...
... 3. Superfamily Manzanelloidea. The only extant family Nucinellidae includes two genera, Nucinella and Huxleyia (Oliver & Taylor, 2012), which collectively formed a clade sister to the Solemyoidea in our phylogeny ( Figure 1). The fossil record suggests that the Manzanelloidea have diverged from the Solemyoidea by the Permian period, when the extinct Manzanella appeared as a possible ancestor of living manzanelloids (Cope, 2000;Pojeta, 1988). ...
Higher systematics and evolutionary history of Protobranchia, a subclass of Bivalvia, have long been controversial due to paucity of prominent shell characters and difficulties in collecting live material for diverse taxa. Here, we evaluate the reliability of shell microstructure for protobranch higher systematics by reconstructing a molecular phylogeny of the subclass. Relationships were assessed using the nuclear (18S rRNA, 28S rRNA and histone H3) and mitochondrial (16S rRNA and cytochrome c oxidase subunit 1) gene sequences from 89 in‐group species. Maximum likelihood reconstruction with the nuclear markers recognized five superfamilies (Nuculoidea, Solemyoidea, Manzanelloidea, Nuculanoidea and Sareptoidea) as the in‐group clades of the monophyletic Protobranchia. Sareptoidea is herein redefined to comprise Sarepta and Setigloma in the sole family Sareptidae, whereas Pristigloma and its monotypic Pristiglomidae are transferred from this superfamily to Nuculanoidea, both in the order Nuculanida. Mapping of shell microstructure characters on the tree confirmed their conservativeness at superfamily level when only living species were taken into account. The Nuculoidea have shells with the outer prismatic and middle/inner nacreous structures; Solemyoidea are characterized by either the radially elongate simple prismatic structure or the reticulate structure in the outer shell layer; Manzanelloidea, Nuculanoidea and Sareptoidea have shells of homogeneous, fibrous prismatic and/or fine complex crossed lamellar structures, all of which lack large structural units. Our Bayesian time calibration, on the contrary, suggested frequent loss of nacre in the Paleozoic and Mesozoic history of Protobranchia, at least once each in Nuculoidea, Manzanelloidea, Solemyoidea and Sareptoidea in the Paleozoic, and perhaps multiple times in Nuculanoidea by the Mesozoic.
... However, Habe (1977) had already suggested that this species might be a synonym of Huxleyia sulcata A. Adams, 1860. Recently, it is becoming clear that two small nucinellids living off Oman possess chemosymbiotic bacteria in their gills (Oliver and Taylor, 2012). This finding confirms the speculation on the symbiosis of some Nucinella species with sulphide-oxidizing bacteria based on their gutless condition (Reid, 1990) and fossil occurrences (Amano et al., 2007a). ...
Many molluscan fossils have been found from the turbidite deposits of the lower Miocene Kurosedani Formation at Kakuma in Toyama City. They include six chemosymbiotic bivalves, namely Solemyidae gen. et sp. indet., Nucinella sp., Lucinoma cf. acutilineatum (Conrad), Conchocele yatsuoensis sp. nov., Pliocardia kawadai (Aoki) and Adulomya chitanii Kanehara. This is the oldest record of chemosymbiotic species in the Japan Sea region. Nucinella has been unknown from the Cenozoic deposits in the Japan Sea borderland and from the Recent Japan Sea. Moreover, the vesicomyids P. kawadai and A. chitanii are shared with those from the lower Miocene Honya Formation in Fukushima Prefecture and from the middle Miocene Nupinai Formation in eastern Hokkaido. This supports our hypothesis that the invasion of chemosymbiotic species from the Pacific side to the Japan Sea took place soon after the formation of a deep-sea basin in the Japan Sea.
... Distribution of newly described species from Discovery cruise 211 over the OMZ of the Oman Margin in relation to depth and dissolved oxygen concentrations. Compiled fromOliver, 2000Oliver, , 2015Holmes, 2006 andTaylor, 2012 ...
The perceived taxonomic uniformity of the Indo-Pacific province is discussed with special reference to the marine faunas of the Indian subcontinent and western Indian Ocean. The deep-sea fauna remains largely unexplored but the Arabian Sea upwelling and related oxygen minimum zones create a strong bathyal zonation and high degree of endemism in the Arabian Sea. The extent of this along the west coast of India remains to be evaluated. The bathyal fauna of the Bay of Bengal exhibits similar zonation and endemicity but the comparisons with the Arabian Sea are few. The abyssal fauna of the Indian Ocean is poorly known but the composition is similar to that of the better known deep Atlantic. Some species appear to be cosmopolitan. The shelf faunas are shown not to be uniform with a mixture of wide-ranging Indo-Pacific species and narrow ranging species to specific subregions. Transition zones are postulated for the coasts of the western Indian Ocean. Oceanographic conditions are discussed as possible mechanisms for isolation and development of regional faunas. Taxonomic congruence and consistency are discussed as factors affecting the interpretation of morphological differences between species and their subsequent role in identifying endemicity. At a finer scale the bivalve faunas of the brackish waters around and adjacent to the Indian subcontinent are reviewed. The endemicity of geographically isolated estuaries, lagoons and backwaters is illustrated and further research is indicated. For each section future directions for malacological research are suggested with that of the molecular identity of morpho-species, reinterpretation of endemicity and exploration of the deep-sea as priorities.
... Micro-and macro-borers commonly leave traces on molluscan shells (Glaub, 1999(Glaub, , 2004Edinger, 2002;Edinger and Risk, 2007;Glaub et al., 2007;Radtke et al., 2011). Microborings and microbial endoliths produced by bacteria, fungi, algae, and foraminifers leave very different microscopic traces (Radtke, 1993;Friedman et al., 1997;Glaub et al., 2007;Tapanila and Ekdale, 2007;Wisshak et al., 2008;Oliver and Taylor, 2011). These microborings are often produced by euendolithic microorganisms which can penetrate actively the shells by chemical dissolution to conform a network of tunnels (while other microorganisms can live in preexisting cavities like pores and fissures with no need to bioerode the shells; Golubic et al., 1981;Glaub et al., 2007). ...
Ichnological investigations were carried out on late Quaternary shells of the intertidal deep infaunal bivalve Tagelus plebeius (Lightfoot, 1786) found along the southwestern Atlantic, between Uruguay and the southernmost Buenos Aires Province in Argentina. Analyses reveal distinctive marks that are spread on the outer shell surface only. The marks are regular–unbranched–elongate, perpendicular to the outer shell growth lines, with deflections on the margins, never interconnected, without bifurcations, conforming bottom–up constructions. They occur in hundreds of specimens from many samples taken from sediments ranging in age from the late Pleistocene to the Recent. These marks have never been reported or described for this species and their origin and formation remain elusive. We describe these traces thoroughly and we propose an explanation for their preservation on about half the shells examined. Potential destructive boring structures (excavated from outside–in) or bioerosion activities by other macro- or micro-organisms are dismissed. These antimarginal asymmetric traces point instead to a process of constructive bioclaustrations (grown from the bottom–up) produced in situ during the life of the bivalve by unknown symbiont organisms. Additionally, the regular pattern observed for the marks exclude host growth as a consequence of abiotic/extrinsic causes. From a palaeoecological perspective, these structures suggest a biotic interaction that was hitherto undescribed neither for bivalves nor for the late Quaternary of the southwestern Atlantic.
