New data on molluscs and their shell microstructures from the Middle Cambrian Gowers Formation, Australia

Abstract: Numerous new cases of preserved shell microstructure were discovered in molluscs from the Middle Cambrian Gowers Formation (Ptychagnostus atavus/Peronopsis opimus Zone, Floran Stage) in the Georgina Basin, Australia. The new data provide further evidence that, by the Middle Cambrian, molluscan shell microstructures were diverse, and many molluscs had a complex shell with multiple types of shell microstructure. In addition, many new occurrences of laminar microstructures are described herein. For many, the nature of these laminar microstructures is not known, but in three species the microstructure is foliated calcite, and in at least two the microstructure is more likely to have been calcitic semi‐nacre, a type of microstructure known in brachiopods and bryozoans but unknown in modern molluscs. This commonality among these three closely related lophotrochozoans underscores a similar mechanism of biomineralization. Moreover, these observations suggest a prevalence of calcite‐shelled lineages among molluscs from the Middle Cambrian, a time of calcite seas. In addition, the broad occurrence of laminar, nacre‐like microstructures in many of these fossils reveals how widespread these strong (fracture‐resistant) microstructures were in Middle Cambrian molluscs. Additionally, a few specimens of Yochelcionella preserve imprints of a bilaterally symmetrical pair of muscle scars. New taxa described here include Corystos thorntoniensis gen. et sp. nov., Yochelcionella snorkorum sp. nov., Yochelcionella saginata sp. nov., and Anhuiconus? agrenon sp. nov.     

The origins of molluscs

The interrelationships and evolutionary history of molluscs have seen great advances in the last decade. Recent phylogenetic studies have allowed alternative morphology‐based evolutionary scenarios to be tested and, most significantly, shown that the aplacophorans are sister group to polyplacophorans (chitons), corroborating palaeontological and embryological evolutionary scenarios in which aplacophorans are secondarily simplified from a chiton‐like ancestor. Aplacophoran morphology therefore does not represent the plesiomorphic condition for molluscs as a whole. The mollusc crown group radiated in the Early Cambrian, and rapidly thereafter, stem lineages to the major molluscan classes emerged: cephalopods, gastropods, bivalves (= pelecypods), monoplacophorans, rostroconchs (inferred stem scaphopods) and aculiferans. This attests to the fast, adaptive radiation of the crown group during the Cambrian explosion. Kimberella from the latest Ediacaran exhibits several molluscan traits, which justifies its position as a molluscan stem‐group member, rather than as a more basal Lophotrochozoan. The interrelationships among the conchiferan molluscs are still a matter of contention and require further palaeontological and molecular phylogenetic scrutiny.     

First record of <Emphasis Type="Italic">Pojetaia runnegari</Emphasis> Jell, 1980 and <Emphasis Type="Italic">Fordilla</Emphasis> Barrande, 1881 from the Middle East (Taurus Mountains,Turkey) and critical review of Cambrian bivalves

Cambrian bivalves from the Middle East are reported here for the first time. They come from early “Middle Cambrian” and latest “Early Cambrian” limestones of the lower Çal Tepe Formation at the type locality (near Seydi?ehir, western Taurides). The majority of the new findings consists of Pojetaia runnegari Jell, 1980, but a few specimens of Fordilla sp. represent the first report of this genus from “Middle Cambrian” strata. Based on a compilation of the hitherto reported, but mostly revised Cambrian bivalves, the today widely accepted taxa are discussed. The genera Pojetaia Jell, 1980 and Fordilla Barrande, 1881 are critically evaluated, and three valid species are included in Pojetaia: P. runnegari Jell, 1980, P. sarhroensis Geyer and Streng, 1998, and—with limitations—P. ostseensis Hinz-Schallreuter, 1995. Fordilla also includes three species: F. troyensis Barrande, 1881, F. sibirica Krasilova, 1977, and F. germanica Elicki, 1994. The Cambrian genera Tuarangia MacKinnon, 1982, Camya Hinz-Schallreuter, 1995, and Arhouriella Geyer and Streng, 1998 most probably belong to the class Bivalvia. Palaeoecologically, the Cambrian bivalves of the Western Perigondwanan shelf seem to occur in a relatively small window of low-energy, subtidal, open-marine, warm-water conditions on a muddy carbonate ramp or platform with reduced sedimentation rate. The frequently interpreted infaunal mode of life of Pojetaia and Fordilla is questioned by observations of similarly organized modern bivalves. The palaeogeographical distribution of Pojetaia and Fordilla is discussed with respect to their early ontogeny and to differences in the recent state of knowledge on shelly fossils from Cambrian carbonate successions of Perigondwana.     

Aragonitic dendritic prismatic shell microstructure in Thracia (Bivalvia,Anomalodesmata)

The shells of most anomalodesmatan bivalves are composed of an outer aragonitic layer of either granular or columnar prismatic microstructure, and an inner layer of nacre. The Thraciidae is one of the few anomalodesmatan families whose members lack nacreous layers. In particular, shells of members of the genus Thracia are exceptional in their possession of a very distinctive but previously unreported microstructure, which we term herein “dendritic prisms.” Dendritic prisms consist of slender fibers of aragonite which radiate perpendicular to, and which stack along, the axis of the prism. Here we used scanning and transmission electron microscopical investigation of the periostracum, mantle, and shells of three species of Thracia to reconstruct the mode of shell calcification and to unravel the crystallography of the dendritic units. The periostracum is composed of an outer dark layer and an inner translucent layer. During the free periostracum phase the dark layer grows at the expense of the translucent layer, but at the position of the shell edge, the translucent layer mineralizes with the units typical of the dendritic prismatic layer. Within each unit, the c‐axis is oriented along the prismatic axis, whereas the a‐axis of aragonite runs parallel to the long axis of the fibers. The six‐rayed alignment of the latter implies that prisms are formed by {110} polycyclically twinned crystals. We conclude that, despite its distinctive appearance, the dendritic prismatic layer of the shell of Thracia spp. is homologous to the outer granular prismatic or prismatic layer of other anomalodesmatans, while the nacreous layer present in most anomalodesmatans has been suppressed.     

STENOTHECOIDA,A PROPOSED NEW CLASS OF CAMBRIAN MOLLUSCA

Cambridium, Bagenovia, and Stenothecoides, composing the Family Cambridiidae, a monotypic superfamily and an order, were in 1960 assigned (although with a query) to the molluscan class Monoplacophora. The basic error of this assignment, according to the author, was the assumption that these specimens are univalves. One specimen from Siberia and a second from Alaska demonstrate that Stenothecoides is bivalved; Bagenovia was first described as a bivalve, but the implication of two valves was ignored. Short internal ridges normal to the shell margin in Cambridium and Stenothecoides, described by Rasetti and Horný, show little resemblance to features of pelecypod shells. These markings are not homologous to paired muscle scars of monoplacophorans. The asymmetric bivalved shell and internal furrows are interpreted as features of class-rank significance; the extinct class Stenothecoida is proposed to accommodate these genera. These animals are most common in Lower Cambrian, but range into Middle Cambrian. They may have been functionally similar to brachiopods, but were unable to compete with those more efficient bivalves.     

Plywood‐like shell microstructures in hyoliths from the middle Cambrian (Drumian) Gowers Formation,Georgina Basin,Australia

Hyoliths are a group of Palaeozoic fossils with calcareous shells whose affinities remain controversial. As their shells were originally aragonitic, their fossils are usually coarsely recrystallized, and few data on their microstructure are available. We report hyoliths from the middle Cambrian (Drumian, Floran) Gowers Formation of the eastern Georgina Basin, Queensland. These are preserved as phosphatic internal moulds, often with the inner layers of the shell also partly replaced by phosphate. Microstructural details preserved by this early diagenetic phosphatization show that these hyolith conchs were originally composed of fibrous crystallites, c. 0.5 μm wide, parallel to one another and to the inner surface of the shell. In several species, the fibres are arranged in a plywood‐like structure composed of multiple lamellae with a different fibre orientation in each lamella: often they are transversely oriented (relative to the long axis of the conch) in the inner part of the wall and longitudinally oriented in the outer part. Opercula also show a microstructure of parallel fibres. The lamello‐fibrillar microstructure we report from hyoliths is reminiscent of microstructures of many Cambrian molluscs; that this microstructure is found in both conchs and opercula suggests that these structures are serial homologues of one another, and in this respect they resemble brachiopod valves. As with many other biological plywoods, the hyolith shell probably records self‐organization in a liquid‐crystal‐like organic matrix. This provided a straightforward way to construct a material that could resist stresses from different directions, offering an effective defence against predators.     

Homologous shell microstructures in Cambrian hyoliths and molluscs

Hyoliths were among the earliest biomineralizing metazoans in Palaeozoic marine environments. They have been known for two centuries and widely assigned to lophotrochozoans. However, their origin and relationships with modern lophotrochozoan clades have been a longstanding palaeontological controversy. Here, we provide broad microstructural data from hyolith conchs and opercula from the lower Cambrian Xinji Formation of North China, including two hyolithid genera and four orthothecid genera as well as unidentified opercula. Results show that most hyolith conchs contain a distinct aragonitic lamellar layer that is composed of foliated aragonite, except in the orthothecid New taxon 1 that has a crossed foliated lamellar microstructure. Opercula are mostly composed of foliated aragonite and occasionally foliated calcite. These blade or lath‐like microstructural fabrics coincide well with biomineralization of Cambrian molluscs rather than lophophorates, as exemplified by the Cambrian members of the tommotiid‐brachiopod linage. Accordingly, we propose that hyoliths and molluscs might have inherited their biomineralized skeletons from a non‐mineralized or weakly mineralized common ancestor rather than as a result of convergence. Consequently, from the view of biomineralization, the homologous shell microstructures in Cambrian hyoliths and molluscs strongly strengthen the phylogenetic links between the two groups.     

Shell nacre ultrastructure and depressurisation dissolution in the deep-sea hydrothermal vent mussel Bathymodiolus azoricus

This study describes the micro-morphological features of the shell nacre in the vent mytilid Bathymodiolus azoricus collected along a bathymetric gradient of deep-sea hydrothermal vents of the mid-Atlantic ridge (MAR). Pressure-dependent crystallisation patterns were detected in animals subjected to post-capture hydrostatic simulations. We provide evidence for the following: (1) shell micro morphology in B. azoricus is similar to that of several vent and cold-seep species, but the prismatic shell layers may vary among bathymodiolids; (2) nacre micro-morphology of mussels from three vent sites of the MAR did not differ significantly; minor differences do not appear to be related to hydrostatic pressure, but rather to calcium ion availability; (3) decompression stress may cause drop off in pH of the pallial fluid that damages nascent crystals, and in a more advanced phase, the aragonite tablets as well as the continuous layer of mature nacre; and (4) adverse effects of decompression on calcium salt deposition in shells was diminished by re-pressurisation of specimens. The implications of the putative influence of hydrostatic pressure on biomineralisation processes in molluscs are discussed. An erratum to this article can be found at     

New data on the enigmatic Ocruranus–Eohalobia group of Early Cambrian small skeletal fossils

Abstract: The Ocruranus–Eohalobia group, whose members were variously considered to be brachiopods, bivalves, chitons, tommotiids and coeloscleritophorans, are difficult to classify because of lack of morphological detail and evidence for skeletal reconstruction. New specimens from South China reveal more information about Ocruranus–Eohalobia and allow progress towards deciphering the skeletal reconstruction and phylogenetic affinity of this enigmatic group. Many specimens have a phosphatic inner and outer coat (mould) with empty space in between that resulted from dissolution of the original shell. Moreover, many of the internal moulds show a previously unknown type of shell microstructure that consisted of stacked layers of highly organized, acicular crystallites that radiated from the apex of the shell towards the aperture. The dissolved shell and needle‐like crystals suggest an original calcareous, probably aragonitic, shell mineralogy. A few specimens also show a polygonal texture in regions that suggests the shell had a thin, prismatic inner shell microstructure. Ocruranus and Eohalobia belong to the same skeleton, and we herein synonymize Eohalobia with the older Ocruranus. Moreover, new specimens from Meishucun reveal a third type of shell plate, similar in form and inferred placement to intermediate valves of chitons. Ocruranus is likely a mollusc, and possibly a member of the chiton stem lineage. If so, then the beginning of the known record of chitons would be extended back from late Cambrian (Saukia Zone; Furongian) to early Cambrian (Meishucunian; Series 1).     

Evidence of predation in Early Cretaceous unionoid bivalves from freshwater sediments in the Cameros Basin,Spain

Here, we present evidence of possible vertebrate predation on freshwater bivalves from the Lower Cretaceous strata of the Cameros Basin (Spain). The described collection contains the largest number of vertebrate‐inflicted shell injuries in freshwater bivalve shells yet reported in the Mesozoic continental record. Several types of shell damage on fossil shells of Protopleurobema numantina (Bivalvia: Unionoida) are described and their respective modes of formation interpreted in the context of morphological attributes of the shell injuries and the inferred tooth morphology of predators that could have inflicted such injuries. Detailed study of these bite marks shows similarities with the well‐documented injuries in the shells of marine molluscs, namely ammonoids, that have likewise been attributed to reptilian predators. The most parsimonious interpretation suggests crocodiles as the vertebrates interacting with the bivalves in the Cameros Basin. □Barremian–Aptian; bite marks; freshwater bivalves; predation; reptile; Unionoida.     

Bryozoans as taphonomic engineers,with examples from the Upper Ordovician (Katian) of Midwestern North America

A combination of encrusting calcitic bryozoans and early seafloor dissolution of aragonitic shells recorded in the Cincinnatian Series of the upper Midwest of North America allowed the preservation of abundant moulds of mollusc fossils bioimmured beneath the attachment surfaces of the bryozoans. We here call this preservational process ‘bryoimmuration’, defined as a bryozoan‐mediated subset of bioimmuration. The bryozoans moulded very fine details of the mollusc shells, usually with more accuracy than inorganic sediment moulds. Most of the bryozoans are heterotrypid trepostomes with robust low‐Mg calcite skeletons. The molluscs are primarily bivalves, gastropods, nautiloids and monoplacophorans with their originally aragonitic shells now dissolved. Many of the encrusting bryozoans are so thin and broad that they give the illusion of calcitic mollusc shells clinging to the moulds. Some molluscs in the Cincinnatian, especially monoplacophorans and epifaunal bivalves, would be poorly known if they had not been bryoimmured. Unlike internal and external moulds in sediment, bryoimmured fossils could be transported and thus record aragonitic faunas in taphonomic assemblages (e.g. storm beds) in which they would otherwise be rare or absent. In addition, bryoimmurations of aragonitic shells often reveal the ecological succession of encrustation on the shells by exposing the earliest encrusters and borings that were later overgrown. Bryoimmuration was common during the Late Ordovician because the calcite sea at the time quickly dissolved aragonitic shells on the seafloor before final burial, and large calcitic bryozoans very commonly used molluscs as substrates. Bryoimmuration is an important taphonomic process for preserving aragonitic faunas, and it reveals critical information about sclerobiont palaeoecology. Several Cincinnatian mollusc holotypes are bryoimmured specimens. Bryozoans involved in bryoimmuration enhance the preservation of aragonitic fauna and thus act as taphonomic engineers.     

Dynamics of sheet nacre formation in bivalves

Formation of nacre (mother-of-pearl) is a biomineralization process of fundamental scientific as well as industrial importance. However, the dynamics of the formation process is still not understood. Here, we use scanning electron microscopy and high spatial resolution ion microprobe depth-profiling to image the full three-dimensional distribution of organic materials around individual tablets in the top-most layer of forming nacre in bivalves. Nacre formation proceeds by lateral, symmetric growth of individual tablets mediated by a growth-ring rich in organics, in which aragonite crystallizes from amorphous precursors. The pivotal role in nacre formation played by the growth-ring structure documented in this study adds further complexity to a highly dynamical biomineralization process.     

Shell microstructures of the Early Cambrian Anabarella and Watsonella as new evidence on the origin of the Rostroconchia

Internal moulds of the laterally compressed monoplacophoran Anabarella plana Vostokova, 1962, and likely earliest rostroconch Watsonella Grabau, 1900, from the Early Cambrian of the Siberian Platform, show similar microstructures. The moulds are covered with a thin phosphatic crust replicating the inner morphology and microstructure of the shells. The shells were completely removed during etching of the samples in 10% acetic acid, except for some moulds of Watsonella sp., which retained an incompletely preserved and recrystallized wall. Three types of microtexture were found in moulds of Anabarella and Watsonella : polygonal, spiny and step-wise. The polygonal texture is well exposed in the apical area and dorsal margin and is interpreted to represent a prismatic outer layer. The polygons can be partially overlapped by spiny and stepwise textures that may represent a crossed-lamellar inner layer. Prisms and lamellae were first-order structural units, probably consisting of fibers. The similar shell microstructures of Anabarella and Watsonella , especially at the dorsal margins, support the hypothesis that a laterally compressed monoplacophoran such as Anabarella plana was the first evolutionary step from monoplacophorans towards Early Cambrian bivalves via the earliest rostroconch-like Watsonella.     

Shell nacre ultrastructure and depressurisation dissolution in the deep-sea hydrothermal vent mussel <Emphasis Type="Italic">Bathymodiolus azoricus</Emphasis>

This study describes the micro-morphological features of the shell nacre in the vent mytilid Bathymodiolus azoricus collected along a bathymetric gradient of deep-sea hydrothermal vents of the mid-Atlantic ridge (MAR). Pressure-dependent crystallisation patterns were detected in animals subjected to post-capture hydrostatic simulations. We provide evidence for the following: (1) shell micro morphology in B. azoricus is similar to that of several vent and cold-seep species, but the prismatic shell layers may vary among bathymodiolids; (2) nacre micro-morphology of mussels from three vent sites of the MAR did not differ significantly; minor differences do not appear to be related to hydrostatic pressure, but rather to calcium ion availability; (3) decompression stress may cause drop off in pH of the pallial fluid that damages nascent crystals, and in a more advanced phase, the aragonite tablets as well as the continuous layer of mature nacre; and (4) adverse effects of decompression on calcium salt deposition in shells was diminished by re-pressurisation of specimens. The implications of the putative influence of hydrostatic pressure on biomineralisation processes in molluscs are discussed.     

Evidence for Palaeozoic orthoconic cephalopods with bimineralic shells

Based on the aragonite composition of extant and exceptionally preserved fossil cephalopods going back to the early Palaeozoic, it is commonly assumed that all externally shelled cephalopods had an aragonitic shell wall. We demonstrate herein that at least two taxa of Siluro‐Devonian orthoconic nautiloids (Dawsonoceras, Spyroceras) had an original bimineralic shell, which developed convergently with gastropods and bivalves.     

Molecular Evolution of Mollusc Shell Proteins: Insights from Proteomic Analysis of the Edible Mussel Mytilus

Shell matrix proteins (SMPs) that are embedded within calcified layers of mollusc shells are believed to play an essential role in controlling the biomineral synthesis and in increasing its mechanical properties. Among the wide diversity of mollusc shell textures, nacro-prismatic shells represent a tremendous opportunity for the investigation of the SMP evolution. Indeed, nacro-prismatic texture appears early in Cambrian molluscs and is still present in the shell of some bivalves, gastropods, cephalopods and very likely also, of some monoplacophorans. One key question is to know whether these shells are constructed from similar matrix protein assemblages, i.e. whether they share a common origin. Most of the molecular data published so far are restricted to two genera, the bivalve Pinctada and the gastropod Haliotis. The shell protein content of these two genera are clearly different, suggesting independent origins or considerable genetic drift from a common ancestor. In order to describe putatively conserved mollusc shell proteins, here we have investigated the SMP set of a new bivalve model belonging to another genera, the edible mussel Mytilus, using an up-to-date proteomic approach based on the interrogation of more than 70,000 EST sequences, recently available from NCBI public databases. We describe nine novel SMPs, among which three are completely novel, four are homologues of Pinctada SMPs and two are very likely homologues of Haliotis SMPs. This latter result constitutes the first report of conserved SMPs between bivalves and gastropods. More generally, our data suggest that mollusc SMP set may follow a mosaic pattern within the different mollusc models (Mytilus, Pinctada, Haliotis). We discuss the function of such proteins in calcifying matrices, the molecular evolution of SMP genes and the origin of mollusc nacro-prismatic SMPs.     

滇东北早寒武世梅树村阶单板类及其新属种研究

本文描述了云南东部早寒武世早期梅树村阶软体动物单板类化石,计有５新属７新种和１个未定种,它们是Ｓｔｒｉａｔｏｃｏｎｕｓ ｙｕｌｕｅｎｓｉｓ ｇｅｎ．ｅｔ ｓｐ．ｎｏｖ．,Ｓｔｒｉａｔｏｃｏｎｕｓ ｓｐ．,Ａｅｇｉｔｅｌｌｕｓ ｃｏｎｃｅｎｔｔｒｉｃｕｓ ｇｅｎ．ｅｔ ｓｐ．ｎｏｖ．,Ｔｕｂａｔｏｃｏｎｕｓ ｙｕｌｕｅｎｓｉｓ ｇｅｎ．ｅｔ ｓｐ．ｎｏｖ．,Ｐａｐｉｌｌｏｃｏｎｕｓ ｅｘｐｌａｎａｔ     

A molecular palaeobiological hypothesis for the origin of aplacophoran molluscs and their derivation from chiton-like ancestors

Aplacophorans have long been argued to be basal molluscs. We present a molecular phylogeny, including the aplacophorans Neomeniomorpha (Solenogastres) and Chaetodermomorpha (Caudofoveata), which recovered instead the clade Aculifera (Aplacophora + Polyplacophora). Our relaxed Bayesian molecular clock estimates an Early Ordovician appearance of the aculiferan crown group consistent with the presence of chiton-like molluscs with seven or eight dorsal shell plates by the Late Cambrian (approx. 501-490 Ma). Molecular, embryological and palaeontological data indicate that aplacophorans, as well as chitons, evolved from a paraphyletic assemblage of chiton-like ancestors. The recovery of cephalopods as a sister group to aculiferans suggests that the plesiomorphic condition in molluscs might be a morphology similar to that found in monoplacophorans.     

How the mollusc got its scales: convergent evolution of the molluscan scleritome

Radiation of dramatically disparate forms among the phylum Mollusca remains a key question in metazoan evolution, and requires careful evaluation of homology of hard parts throughout the deep fossil record. Enigmatic early Cambrian taxa such as Halkieria and Wiwaxia (in the clade Halwaxiida) have been proposed to represent stem‐group aculiferan molluscs (Caudofoveata + Solenogastres + Polyplacophora), as complex scleritomes were considered to be unique to aculiferans among extant molluscs. The ‘scaly‐foot gastropod’ (Neomphalina: Peltospiridae) from hydrothermal vents of the Indian Ocean, however, also carries dermal sclerites and thus challenges this inferred homology. Despite superficial similarities to various mollusc sclerites, the scaly‐foot gastropod sclerites are secreted in layers covering outpockets of epithelium and are largely proteinaceous, while chiton (Polyplacophora: Chitonida) sclerites are secreted to fill an invaginated cuticular chamber and are largely calcareous. Marked differences in the underlying epithelium of the scaly‐foot gastropod sclerites and operculum suggest that the sclerites do not originate from multiplication of the operculum. This convergence in different classes highlights the ability of molluscs to adapt mineralized dermal structures, as supported by the extensive early fossil record of molluscs with scleritomes. Sclerites of halwaxiids are morphologically variable, undermining the assumed affinity of specific taxa with chitons, or the larger putative clade Aculifera. Comparisons with independently derived similar structures in living molluscs are essential for determining homology among fossils and their position with respect to the enigmatic evolution of molluscan shell forms in deep time. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 949–954.     

The evolution of molluscan photosymbioses: a critical appraisal

Partnerships between animals and photosynthesizing microbes have evolved repeatedly, although their history, adaptations, and ecology remain controversial and little understood. In a critical review of 17 fossil and living clades of shell‐bearing molluscs with photosymbionts (two of them newly inferred), adaptive shell modifications and ecological aspects are discussed in the broader context of photosymbioses in other phyla. Fossil candidates have characteristics that are rare or unknown in living photosymbiotic molluscs, including cementation, porous shell microstructure, and epifaunal habits on carbonate muds. Many ancient photosymbioses may have lived in planktonically more productive environments than are typical of living tropical forms. This may be related to the late appearance (Early Eocene) of the dinoflagellate Symbiodinium, which can thrive under highly oligotrophic conditions. Living photosymbiotic molluscs represent a small and atypical sample of all the photosymbiotic clades that have evolved. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 497–511.