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Non-Lithistid Fossil Demospongiae – Origins of Their Palaeobiodiversity and Highlights in History of Preservation

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Non-Lithistid Fossil Demospongiae – Origins of Their Palaeobiodiversity and Highlights in History of Preservation Systema Porifera: A Guide to the Classification of Sponges, Edited by John N.A. Hooper and Rob W.M. Van Soest © Kluwer Academic/Plenum Publishers, New York, 2002 Non-Lithistid Fossil Demospongiae – Origins of their Palaeobiodiversity and Highlights in History of Preservation Joachim Reitner1 & Gert Wörheide2 1 Geowissenschaftliches Zentrum Göttingen GZG, Abt. Geobiologie, Universität Göttingen, Goldschmidtstr. 3, D-37077 Göttingen, Germany. ([email protected]) 2 Queensland Museum, P.O. Box 3300, South Brisbane, Qld, 4101, Australia. ([email protected]) Available evidence suggests that the first demosponges occur in the Late Proterozoic, with forms characterized by bundles of long mon- axonic spicules. In the Middle Devonian the first modern forms of Dendroceratida, ‘axinellids’ (mostly halichondrids), and first hap- losclerids appeared. An important boundary for the demosponges is the Late Devonian extinction event, which caused a complete overhaul of demosponge communities. The Late Permian and the Triassic, especially the Late Triassic, are the main eras for coralline demosponge radiation and dominance, in which some modern taxa occur for the first time (Ceratoporella, Astrosclera, Vaceletia). In the Late Jurassic the freshwater environments were occupied by certain (marine) demosponges, mostly Haplosclerida. The importance of coralline demosponges as primary reef-builders decreases up to the Late Cretaceous. Keywords: Porifera; Demospongiae; fossil taxa; coralline demosponges. INTRODUCTION most significantly, the discrete siliceous spicules that are often cru- cial to taxonomic identification. The silica of spicules is replaced Demospongiae are an important group of sessile benthic organ- by other minerals, mostly calcite or secondary silica or pyrite. isms showing a special potential for fossil preservation. Up to Isolated spicules are common in certain deposits and some of them 60% of their biomass consists of microorganisms, predominantly are of taxonomic and phylogenetic importance, but only few stud- bacteria, in some cases Archaea, and partly of anaerobic taxa ies have yet been made, especially of the phylogenetically impor- (sulfate-reducing bacteria (SRB) and Archaea) (Reitner & tant Early Palaeozoic strata. In special fossil lagerstätten, like the Schumann- Kindel, 1997). The SRB play a central role in the forma- Burgess shale deposits, entirely preserved sponges are present. tion of Porifera-rich mud mounds and certain microbialites. To a Similarly, one of us (JR) has recently discovered entirely preserved great extent the micrite in these structures was formed by various non-lithistid demosponges in Cambrian and Middle Devonian types of sponge related microorganisms, (and/or) degraded and re- microbialites. Due to the large numbers of sponge-related bacteria organized organic material originated from sponges (Reitner et al., in many demosponges the sponge tissue may mineralize rapidly, 1995), but some portions of these build-ups are also influenced by controlled by sulfate reduction and/or ammonification. In this par- seeps and seepage. In the Upper Devonian a fundamental push in the ticular case certain sponge biomarkers (chemofossils) are pre- development of sponges took place, from the long-existing, stem- served and thus allow chemotaxonomic examination. group Palaeozoic taxa to modern groups of which the monophyla are This chapter does not provide a complete overview on fossil still present. The driving forces for this change are so far unknown, demosponges – which could occupy a volume in itself, and will be but most likely include medium-term fundamental oceanic changes more comprehensively addressed in the forthcoming revision of (water chemistry, nutrient situation) producing new niches for new the Treatise of Invertebrate Paleontology (J.K. Rigby et al., edi- taxa, especially in deeper water and other protected areas. Porifera- tors). The purpose of this chapter is to demonstrate some highlights rich build-ups and black shale environments provide a window to in the history of palaeontological preservation, which provides a answer this question, which concerns reef-like structures, rich in general overview on the early development of the main mono- micrites, without a metazoan framework. This increase in nutrient phyletic groups of non-lithistid demosponges. Some coralline input could have impacted significantly on oceanic environments, sponge taxa are also included in this treatment, but these taxa are possibly through a significant increase of alkalinity as well as restricted to those with modern representatives and those that rep- by increased input of hydrothermal calcium and other metal resent important phylogenetic lines. cations. Porifera react very rapidly to such changes, whereas sponge- associated bacteria are even more sensitive to changes within the general nutrient environment (eutrophism of organic and inorganic PHYLOGENETIC ASPECTS nutrients), as we know from field experiments on modern Porifera. In this way, the rapid development during the Devonian of the poly- New data suggest that ‘sponges’ are probably not mono- phyletic coralline sponges (the so-called ‘sclerosponges’) may have phyletic (Borchiellini et al., 2001), with Calcarea indicated to have been a reaction to the global oceanic change during this critical inter- greater similarities with Cnidaria (perhaps the Ctenophores) than val, and linked with increasing alkalinity and /or massive increase of to sponges with siliceous skeletons. These data include nucleic the overall Ca2ϩ dissolved in ocean water (Arp et al., 2001). acid analysis (18s rDNA), the spectra of fatty acids and the occur- Little is known about the fossil record of non-lithistid demo- rence of sponge-related bacteria. In these latter characters the sponges, in contrast to the ‘lithistid’ demosponges, and taxa with a Calcarea do not exhibit the very characteristic long-chained demo- secondary calcareous basal skeleton, due to the poor preservation spongic acids, which are very good biomarkers for all demo- potential of the soft tissue, the collagenous spongin skeleton and, sponges and hexactinellids (Thiel et al., 2001), and in most 52 Porifera • Demospongiae • Non-Lithistid Demosponges 53 Calcarea mesohyle bacteria are missing. This evidence certainly A suggests a more distant phylogenetic position for the Calcarea, although it does not necessarily imply sponge paraphyly. Demosponges demonstrate the following clades based on morphological characters: (1) Homosclerophorida. (2) Tetractinomophora, including the Astrophorida, Spirophorida and Hadromerida. (3) Ceractinomorpha, including the aspicular Dendroceratida, Dityoceratida and Verongida (so-called ‘Keratosa’) and spicu- lose taxa like the Poecilosclerida, Haplosclerida, Halichondrida (‘Axinellida’) and Agelasida. THE CONCEPT OF SPONGE-BIOFILMS The origin of the sponge bauplan is probably related to the development of special stromatolite-forming biofilms during the B Early Proterozoic – at the same time as endosymbioses of eukary- otic cells evolved. This hypothesis is supported by direct evidence from 1.8 billion year old stromatolites containing sponge-specific C30 steranes and 24-isopropylcholestanes (Moldowan et al., 1994a,b), which are extremely abundant in demosponges and therefore good biomarkers for these animals (Thiel, 1997). A fur- ther indirect argument for a phylogenetic relationship between the modern morphology of sponges and ancestral biofilms is the pres- ence of mid-chain branched carboxylic acids (MBCA) in modern demosponges, which are probably related to anaerobic sulfate- reducing bacteria within the sponge mesohyl (Thiel et al., 1999). This type of bacterial biomarker was previously unknown in any other marine environment but was recently discovered in het- erotrophic biofilms of the modern highly alkaline Walker Lake in Nevada. We hypothesise that Early Proterozoic oceanic environ- ments had a higher alkalinity than Recent seas (Kempe & Kazmierzcak, 1994), and thus the occurrence of certain species of bacteria adapted to alkaline environments found in modern demo- sponges – especially in bacteria-rich demosponges like the possi- ble ancestral astrophorid taxon Geodia – supports this assumption. Our working hypothesis – that sponges are highly developed biofilms with a close relationship to choanoflagellate eukaryotic cells – is based on the analysis of the sponge-related microorgan- isms and biofilm analyses from extreme environments. Demosponges exhibit a mesohyle community of Eubacteria, mainly gamma and alpha proteobacteria, few gram-positive bacteria and only in a few cases the Archaea (Schumann-Kindel et al., 1997). In contrast to the demosponges all taxa of the Hexactinellida demonstrate a community of microorganisms dominated by Archaea (Thiel et al., 2001). PALAEONTOLOGICAL HISTORY OF DEMOSPONGES Late Proterozoic Demosponge Remains Fig. 1. A, Late Proterozoic (ca. 555my) sponge with demosponge affini- The spicule record of sponges starts in the Late Proterozoic. In ties from the Cloudina-reefs of the Kuibis Formation (Zebra River, most cases these are simple monaxonic types with uncertain affini- Southern Namibia). The small sponges with tylostyle-type spicules are ties. Some of them show hexactinellid affinities with simple hexa- located between Cloudina-tubes. Cloudina has probably pogonophoran ctines and stauractines. The oldest spicules with demosponge affinites and represents the first organism in earth history with a calcified skeleton – onset of biomineralisation.
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