Short Communication

A hypercalcified sponge with soft relatives: Vaceletia is a keratose demosponge

Stromatoporoids are common shallow marine hypercalcified sponges in two major episodes with distinctive skeletal architectures: 1) Palaeozoic: Ordovician to Late Devonian; and 2) Mesozoic: Late Triassic to Cretaceous and rare Cenozoic, but not confirmed in Permian and earlier Triassic strata. Stromatoporoids appeared in Early to Middle Ordovician strata, important in buildups from late Middle Ordovician metazoan expansions (part of the Great Ordovician Biodiversification Event). Throughout the Palaeozoic, some stromatoporoid taxa occur across several palaeocontinents, and, if they are the same biological taxa, presumably migrated as larvae across oceans. Palaeozoic stromatoporoids suffered 5 events of decline; Event 1): end-Ordovician Mass Extinction; surviving forms are typical Silurian taxa, marking change of abundance from labechiid to clathrodictyid forms. Event 2): late Silurian to Early Devonian contraction: stromatoporoids became scarce with low generic diversity, presumably related to global sea-level fall. Intra-Silurian extinction events principally affected conodonts and graptolites, associated with positive carbon isotope excursions, but not stromatoporoids, likely because of their shallow marine benthic habit, contrasting pelagic oceanic planktonic and nektonic fauna influenced by oceanographic changes. Stromatoporoid expansion to their late Early to Middle Devonian (Eifelian and Givetian) acme, forming a major Phanerozoic global reef system, was likely linked to global sea-level rise, when epeiric seas expanded, but followed by Event 3): end-Givetian extinction, possibly related to cooling; Event 4): Frasnian-Famennian (FF) extinction; and Event 5): end-Devonian (Hangenberg Event) extinction; 4 and 5 may be related to sea-level fall, cooling, anoxia and potentially, magmatism. The apparent stratigraphic gap between end-Devonian and Triassic stromatoporoids was not extinction of Palaeozoic stromatoporoids, because rare Carboniferous examples in England, Russia, USA and Japan prove survival in shallow marine environments. Prior interpretation that stromatoporoid-grade sponges lost ability to calcify is unlikely, because chaetetid hypercalcified sponges expanded and built Carboniferous reefs. Important is that skeletal architectures of stromatoporoid and chaetetid hypercalcified sponges are regarded as ‘grades of organisation’ of the skeleton, lacking phyletic value; living stromatoporoid- and chaetetid-grade sponges occur in the classes Demospongiae and Calcarea based on their spicules. This implies that extinction of sponge taxa that just happened to have been stromatoporoid-grade hypercalcifiers may explain stromatoporoid loss in the end-Devonian, and may point to unpreserved crises in non-calcifying Porifera, noting poor sponge records in end-Devonian strata. Having also survived the end-Permian and end-Triassic extinctions, stromatoporoid-grade hypercalcification expanded again in the Jurassic, together with sphinctozoan and inozoan grades, and then survived the K-Pg extinction although stromatoporoid-grade sponges are rare after the Cretaceous, perhaps due to the large progressive sea-level fall of the Cenozoic and consequent loss of habitat. Stromatoporoids appear to be more abundant during calcite seas times, so there may be both an oceanographic chemical control on their development and a preservation bias towards calcite rather than aragonite mineralogy. Overall, the ability of sponges to hypercalcify was not lost throughout their Phanerozoic history; thus, stromatoporoids and other hypercalcified sponges are preserved evidence of the resilience of sponges to environmental change, in contrast other famous reef-building forms, such as tabulate and rugose corals, and rudist bivalves, which became extinct.

Sponges represent one of the most species-rich hosts for commensal barnacles yet host utilisation and diversity have not been thoroughly examined. This study investigated the diversity and phylogenetic relationships of sponge-inhabiting barnacles within a single, targeted host group, primarily from Western Australian waters. Specimens of the sponge order Dictyoceratida were surveyed and a total of 64 host morphospecies, representing four families, were identified as barnacle hosts during the study. Utilising molecular (COI, 12S) and morphological methods 42 molecular operational taxonomic units (MOTUs) of barnacles, representing Acasta, Archiacasta, Euacasta and Neoacasta were identified. Comparing inter- and intra-MOTU genetic distances showed a barcode gap between 2.5% and 5% for COI, but between 1% and 1.5% in the 12S dataset, thus demonstrating COI as a more reliable barcoding region. These sponge-inhabiting barnacles were demonstrated to show high levels of host specificity with the majority being found in a single sponge species (74%), a single genus (83%) or a single host family (93%). Phylogenetic relationships among the barnacles were reconstructed using mitochondrial (12S, COI) and nuclear (H3, 28S) markers. None of the barnacle genera were recovered as monophyletic. Euacasta was paraphyletic in relation to the remaining Acastinae genera, which were polyphyletic. Six well-supported clades of molecular operational taxonomic units, herein considered to represent species complexes, were recovered, but relationships between them were not well supported. These complexes showed differing patterns of host usage, though most were phylogenetically conserved with sister lineages typically occupying related hosts within the same genus or family of sponge. The results show that host specialists are predominant, and the dynamics of host usage have played a significant role in the evolutionary history of the Acastinae.

The term keratolite is proposed for keratosan sponge carbonate dominated by vermiform fabric that preserves the outlines of the original spongin skeleton. Thinly (<~2 cm) interlayered keratosan–microbial carbonate consortia in peritidal sediments near the Cambrian–Ordovician boundary in Newfoundland, Canada, are macroscopically indistinguishable from stromatolites. These carbonate domes and columns consist of approximately equal proportions of keratolite and stromatolite. The keratolite is characterized by pervasive microscopic vermiform fabric, which reflects the original spongin framework. The stromatolite is characterized by fine-grained carbonate with cross-cutting laminae, which primarily formed by sediment trapping. The intimate association of keratolite and stromatolite in these deposits indicates that the sponges and microbes involved shared similar environmental tolerances and requirements. Synchronicity of sponge colonization, followed by stromatolite regrowth, across adjacent columns suggests coordinated responses by both sponges and microbes to local ecophysiological stimuli. Due to their macroscopic similarity, keratolite and fine-grained stromatolite may commonly have been confused with one-another throughout the Phanerozoic, and possibly longer.

Sponges are one of the critical groups in understanding the early evolution of animals. Traditional views of these relationships are currently being challenged by molecular data, but the debate has so far made little use of recent palaeontological advances that provide an independent perspective on deep sponge evolution. This review summarises the available information, particularly where the fossil record reveals extinct character combinations that directly impinge on our understanding of high-level relationships and evolutionary origins. An evolutionary outline is proposed that includes the major early fossil groups, combining the fossil record with molecular phylogenetics. The key points are as follows. (1) Crown-group sponge classes are difficult to recognise in the fossil record, with the exception of demosponges, the origins of which are now becoming clear. (2) Hexactine spicules were present in the stem lineages of Hexactinellida, Demospongiae, Silicea and probably also Calcarea and Porifera; this spicule type is not diagnostic of hexactinellids in the fossil record. (3) Reticulosans form the stem lineage of Silicea, and probably also Porifera. (4) At least some early-branching groups possessed biminerallic spicules of silica (with axial filament) combined with an outer layer of calcite secreted within an organic sheath. (5) Spicules are homologous within Silicea, but also between Silicea and Calcarea, and perhaps with Homoscleromorpha. (6) The last common ancestor of extant sponges was probably a thin-walled, hexactine-bearing sponge with biminerallic spicules. (7) The stem group of sponges included tetraradially-symmetric taxa that grade morphologically into Cambrian fossils described as ctenophores. (8) The protomonaxonid sponges are an early-branching group, probably derived from the poriferan stem lineage, and include the problematic chancelloriids as derived members of the piraniid lineage. (9) There are no definite records of Precambrian sponges: isolated hexactine-like spicules may instead be derived from radiolarians. Early sponges had mineralised skeletons and thus should have a good preservation potential: the lack of sponge fossils in Precambrian strata may be due to genuine absence of sponges. (10) In contrast to molecular clock and biomarker evidence, the fossil record indicates a basal Cambrian diversification of the main sponge lineages, and a clear relationship to ctenophore-like ancestors. Overall, the early sponge fossil record reveals a diverse suite of extinct and surprising character combinations that illustrate the origins of the major lineages; however, there are still unanswered questions that require further detailed studies of the morphology, mineralogy and structure of early sponges.

Most marine sponges precipitate silicate skeletal elements, and it has been predicted that they would be among the few “winners” among invertebrates in an acidifying, high-CO₂ ocean. But members of Class Calcarea and a small proportion of the Demospongiae have calcified skeletal structures, which puts them among those calcifying organisms which are vulnerable to lowered pH and CO₃⁼ availability. A review of carbonate mineralogy in marine sponges (75 specimens, 32 species), along with new data from New Zealand (42 specimens in 15 species) allows us to investigate patterns and make predictions. In general sponges show little variability within individuals and within species (± 0.5 wt.% MgCO₃ in calcite). Extant sponges in Class Calcarea generally produce calcitic spicules with relatively high Mg contents, up to 15 wt.% MgCO₃. Whereas most of the calcifying demosponges are aragonitic, the genus Acanthochaetetes in the order Hadromerida produces extremely high-Mg calcite (14 to 18 wt.% MgCO₃). There is generally a weak phylogenetic consistency among classes, orders and families. Statistical analyses, including those accounting for these phylogenetic effects, fail to find a substantial or significant effect of water temperature on mineralogical variation. In the context of global ocean acidification, sponges which produce high-Mg calcite and/or aragonite will be most vulnerable to dissolution, meaning that not all sponges will be “winners” in a high-CO₂ ocean.

Systematics is nowadays facing new challenges with the introduction of new concepts and new techniques. Compared to most other phyla, phylogenetic relationships among sponges are still largely unresolved. In the past 10 years, the classical taxonomy has been completely overturned and a review of the state of the art appears necessary. The field of taxonomy remains a prominent discipline of sponge research and studies related to sponge systematics were in greater number in the Eighth World Sponge Conference (Girona, Spain, September 2010) than in any previous world sponge conferences. To understand the state of this rapidly growing field, this chapter proposes to review studies, mainly from the past decade, in sponge taxonomy, nomenclature and phylogeny.

In a first part, we analyse the reasons of the current success of this field. In a second part, we establish the current sponge systematics theoretical framework, with the use of (1) cladistics, (2) different codes of nomenclature (PhyloCode vs. Linnaean system) and (3) integrative taxonomy. Sponges are infamous for their lack of characters. However, by listing and discussing in a third part all characters available to taxonomists, we show how diverse characters are and that new ones are being used and tested, while old ones should be revisited. We then review the systematics of the four main classes of sponges (Hexactinellida, Calcispongiae, Homoscleromorpha and Demospongiae), each time focusing on current issues and case studies. We present a review of the taxonomic changes since the publication of the Systema Porifera (2002), and point to problems a sponge taxonomist is still faced with nowadays. To conclude, we make a series of proposals for the future of sponge systematics. In the light of recent studies, we establish a series of taxonomic changes that the sponge community may be ready to accept. We also propose a series of sponge new names and definitions following the PhyloCode. The issue of phantom species (potential new species revealed by molecular studies) is raised, and we show how they could be dealt with. Finally, we present a general strategy to help us succeed in building a Porifera tree along with the corresponding revised Porifera classification.