Article: Exceptional preservation of a novel gill grade in large Cretaceous inoceramids: systematic and palaeobiological implications

Organised mineralised structures observed in large inoceramids (valves on a metre scale) from the Late Albian, Toolebuc Formation, Australia (Inoceramus sutherlandi McCoy, 1865), and the Santonian, Niobrara Formation, USA (Platyceramus sp.), were investigated using variable pressure scanning electron microscope (SEM) with energy-dispersive X-ray spectroscopy (EDX), X-ray microcomputed tomography (micro-CT) and X-ray diffraction (XRD) analyses. These indicate that the structures comprised a phosphate framework of aligned tubes and shallow troughs overlain perpendicularly by evenly spaced structures. In the Toolebuc Inoceramus, these are U-shaped cross-structures, whilst in the Niobrara Platyceramus, they comprise bundled fibre elements. Comparison with modern bivalves indicates that the observed phosphatised structures represent soft-tissue preservation of the gills, as suggested in earlier publications. The tubes and troughs are remnants of a filamental support framework comprising ordinary and primary filaments, whilst the U-shaped cross-structures (I. sutherlandi) and fibrous bands (Platyceramus) represent preserved longitudinal gill musculature. Internal perforate and strand-like fabric observed on the internal surface of some Platyceramus tubular structures suggests that the framework comprised collagen. The presence of primary and ordinary filaments in numerous unusually large plicae, in at least two lamellae, indicates that the gill structures were heterorhabdic. Each plica has at least 40 ordinary filaments, an exceptional number when compared with the maximum of 20 present in modern heterorhabdic gills. The absence of incontrovertible interfilament junctions makes it difficult to say whether inoceramids were filibranch, pseudolamellibranch or eulamellibranch. However, structures that are best attributed to intraplical junctions between filaments suggest the Inoceramidae had gills akin to those of pseudolamellibranch bivalves, although their unusually large number of filaments per plica is more reminiscent of homorhabdic eulamellibranch gills. The general form of the gill is similar to that described in some other pteriomorphs, most specifically Pteria. However, it has more complex junctions and interconnections, although these are not as intricate or pervasive as those observed in the pseudolamellibranch Ostreidae. The connections and well-developed filament framework allowed the gill to reach its unusually large size, supporting the large size of these inoceramid species. The unusually large size of the gill and its components indicate that the organism fed on the larger suspended organic particles in the water column. It would also have been capable of processing large volumes of water quickly, leading to greater potential for food accumulation and with likely implications for respiratory efficiency. This may help explain the common association of inoceramids with oxygen-deficient palaeoenvironments, particularly as the general structure of the inoceramid gill is very different to that observed in the commonest extant chemosymbiotic bivalves.