, Volume 38, Issue 1, pp 1-88

The reef cave dwelling ultraconservative coralline demospongeAstrosclera willeyana Lister 1900 from the Indo-Pacific

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Summary

Astrosclera willeyana Lister 1900 is a pyriform-half spherical, predominantly bright orange colored, coralline demosponge with a mean size of about 20 mm in height and maximum head diameter. The habitat ofAstrosclera is generally restricted to cryptic and light reduced environments of the Indo-Pacific, found mainly in reef caves, but sometimes also in the dim-light areas of cave entrances and overhangs, where it is green colored at the side towards the light. Caves of Indo-Pacific coral reefs were divided into four major facies zones, named 1 to 4 with decreasing light intensities.Astrosclera occurs in reef caves on a carbonate basement in Zone 2, 3, and 4, reaching maximum abundance in Zone 3 and the proximal part of Zone 4, but rare in the distal, very dark areas of Zone 4. Other abundant coralline sponges in reef caves areSpirastrella (Acanthochaetetes) wellsi andVaceletia crypta. Astrosclera is the most common coralline sponge throughout the studied sites of the Indo-Pacific.

The living tissue ofAstrosclera penetrates the basal skeleton to a maximum of 50% depending on specimen size. The soft tissue shows a stromatoporoid grade of organization and can be divided into three major zones. The ectosome is the area directly beneath the exopinacoderm reaching a thickness of about 100–300 μm. The ectosome is characterized by the absence of choanocyte chambers, an enrichment of storage and supporting cells (SSC's), and the archaeocyte-like large vesicle cells (LVC's), which are responsible for the initial formation of aragonitic spherulites. Megasclerocytes were only rarely observed, but show remarkably numerous cytoplasmatic digitations. The choanosome, contiguous with the ectosome but with a more-or-less sharp transition, comprises the major part of the living tissue inAstrosclera, characterized by small choanocyte chambers (±15 μm diameter) and a high density of bacterial symbionts. Other cellular components of the choanosomal mesohyle are archaeocytes, typical pluripotent, phagocytotic demosponges cells, SSC's, and rare fiber cells. Bacteriocytes, which inhabit up to 30 bacteria in a large vacuole, are described for the first time from coralline sponges, as well as a new cell type, the ‘waste cell’, characterized by a large vacuole which is filled up with a fluffy substance, probably non-digested remains of bacteria (membranes, fibrilar EPS). These cells probably derive from archaeocytes or bacteriocytes and are often observed close to excurrent canals. Most of the ground substance of the choanosome lacks collagen and spongin, but has abundant polysaccharide mucus (EPS) produced by the symbiotic bacteria. The zone of epitaxial backfill (ZEB) is considered as a subzone of the choanosome due to its important role for thesyn vivo cementation of the lowest parts of the basal skeleton. It is characterized by a reduced number (or absence) of choanocytes and bacteria and sometimes an enrichment of SSC's.

Astrosclera has a viviparous mode of reproduction. The bacterial symbionts are transferred from the parent sponge in the parenchymella larvae. A large proportion of the population inhabit the choanosome, where the bacteria can reach up to 70% of the total biomass in some areas. The ectosome is nearly free of bacteria. Four major bacterial morphotypes are recognized. Bacteria act either as a direct food source for the sponge (archaeocytes), or the sponge benefits from certain metabolic products of the bacteria (bacteriocytes). Bacteria are at least in part facultative anaerobic, eliminating metabolic waste products of the sponge through fermentative processes during times of reduced or ceasated pumping, or at any time.

The spicular skeleton ofAstrosclera consists of megascleres; microscleres are absent. The basic spicule type is a sub-verticillate—verticillate acanthostyle, of theAgelas type, with a mean length of 80 μm. The spicule morphology and size is highly variable, depending on the geographic origin of the specimen. At the broader proximal end of the spicule (showing a thickening in nearly all populations) the spicule is embedded in spongin microfibrils. As the sponge grows, the spicules get entrapped in the basal skeleton, initially at the proximal end. Based on similar spicule morphology, six ‘groups with similar spicule morphology’ (GSSM's) are differentiated. These GSSM's probably represent geographic sub-species.

Restriction fragment length analysis of the ribosomal DNA (ITS1, 5.8S, ITS2, and small parts of the 18S and 28S regions) was analyzed to test the genetic variation of twenty speciments from five geographical distinct areas (representing three of the GSSM groups based on the spicule morphology). However, the restriction fragment length analysis did not detect any genetic differences that would indicate that there is more than one species ofAstrosclera amongst the specimens examined.

The aragonitic calcareous basal skeleton ofAstrosclera is composed of 20–60 μm-sized aragonitic spherulites, produced by a combination of three processes. First, the spherulites are formed in LVC's in the ectosome. In a second process, the basopinacocytes transport the spherulites to the tips of the skeletal pillars, where they fuse together by epitaxial growth; and in a third process, during upward growth, the soft tissue is slowly rejected from the lowermost-parts of the skeletal cavities and the remaining spaces are subsequently filled by epitaxially-growing aragonite fibers. It is hypothesized thatAstrosclera is able to control the rate of calcification by the regulation of its bacterial population. The mean growth rate ofAstrosclera was measured at 230 μm per year.

Aminoacid and monosaccharide composition of the insoluble intracrystalline matrix (IOM) of the largestAstrosclera ever found (with a maximum age of 550 years) is very stable in all portions of the skeleton. No strong diagenetic effect on the IOM is visible due to the stable composition in all parts of the skeleton, in contrast to the SOM which shows strong diagenetic effects with increasing age of the skeleton, both in aminoacid and monosaccharide composition and quantity. The IOM is dominated by proteins and is represented by the intravacuolar fibers and sheets forming the containers for the seed crystals in the first intracellular process of biocalcification. The nature of the IOM during the second and third process remains unknown without further investigation. Collagen was not detected as a major part of the IOM. The character of the SOM is very typical for Ca2+ binding mucus substances. Two proteins present in the SOM were detected by HPLC gel filtration chromatography, visible at 280 nm wave length detection: a large molecule with a molecular weight of 130 kD, and a smaller one with about 40 kD. Both macromolecules are attributed to have a different function in the biocalcification processes.

Stable isotope time series (46 samples) of δ18O and δ13C were measured in successive growth layers of the largeAstrosclera from Ribbon Reef#10 (GBR).Astrosclera forms its skeletal aragonite in equilibrium with the ambient seawater, and represents, therefore, a high precision recorder of the isotopic history of the ambient seawater. δ13C of surface water dissolved inorganic carbon in the northern Great Barrier Reef has apparently decreased continuously since the mid-16th century. The total decrease is 0.7‰. The major decline of 0.5‰ occurred during the industrial period of the 19th and 20th century, likely to be due to the increased release of CO2 by deforestation and burning of fossil fuel during the period of industrialization after 1850 (increased input of lighter carbon isotopes). The oxygen isotope history shows a slightly colder (and/or dryer) phase before 1850, which correlates with the Little Ice Age. A considerable shift to lighter values occurred during the 20th century (warming of SST). This may be due to an anthropogenic greenhouse effect. Most of the major climatic changes caused by ENSO/El Niño events as well as by large volcano eruptions in the last four and a half centuries were recorded in the oxygen isotope record ofAstrosclera.

A large number of sponges with spherulitic microstructures were observed in the Triassic deposits of St. Cassian (Carnian, Dolomites) and of the Alacir Clay Valley near Antalya (lower Norian, Turkey). At least some of the sponge skeletal morphologies, certainly belonging to different taxa thanAstrosclera, appear to have been formed by the same processes as observed in extantAstrosclera. It was found that morphological characters of the ‘spherulitic skeleton’, even though they show signs of same formation processes, have no higher taxonomic value. The spherulitic skeleton must have had appeared independently in different lineages, and thus can be regarded as a convergent character.

Although the spherulitic basal skeleton was determined to have no higher taxonomic value, it was nevertheless used to identify sponges with affinities to the extantAstrosclera, since the Triassic ‘astrosclerid’ sponges lack spicules. Only one type of sponge belonging to the taxonAstrosclera was found in the Triassic deposits of Antalya. This sponge shows a gross morphology similar to extantA. willeyana, and all the features of the three distinct biocalcification processes leading to the formation of the basal skeleton are present. Spicules, thick, short subacanthostyles/styles, were found in this specimen. A new species,Astrosclera cuifi n. sp. is described in this present work, and it is shown that the ultraconservative taxonAstrosclera has persisted at least since the late Triassic.