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<I>Spongia</I> (Porifera, Demospongiae)

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<I>Spongia</I> (Porifera, Demospongiae) BULLETIN OF MARINE SCIENCE, 63(2): 317–328, 1998 MORPHO-FUNCTIONAL ADAPTATIONS OF THREE SPECIES OF SPONGIA (PORIFERA, DEMOSPONGIAE) FROM A MEDITERRANEAN VERTICAL CLIFF Roberto Pronzato, Giorgio Bavestrello and Carlo Cerrano ABSTRACT Spongia virgultosa, S. officinalis and S. agaricina probably arise from a single ances- tor and, at present, colonize three different habitats along the Portofino Promontory cliff and deep rocks (Ligurian Sea, Italy) from the first 2–3 m to 100 m depth. S. virgultosa evolved an encrusting shape to face the high water movement of shallow coastal water, whereas the two shapes (elephant-ear or vase) of S. agaricina are related to the interac- tion with the local water movement and the consequent sediment transport. S. officinalis is more variable in shape and more euryoecious than the others. The network of secondary skeleton fibers shows no ultrastructural difference in the three species: the primary fibers, however, are lacking in S. virgultosa, being present only in conules in S. officinalis and forming a well developed network in S. agaricina, which crosses the whole width of the sponge. The three sponges interact in different ways with foreign matter, showing different abilities of particle selection, together with a morpho- logic plasticity linked to water movement. The skeletons of the species of Spongia are characterized by a strong, soft network of spongine fibers; foreign materials, such as sand grains and allocthonous spicules, are normally included in the primary fibers (Vacelet, 1959; de Laubenfels, 1948). This incor- poration aptitude, confers differential skeletal stiffness in the various species. Among demosponges, the lack of spicules and skeleton composed of a soft network of spongin is considered a derived character (Hartman,1982; Van Soest, 1991). Sponges have a high phenotypic plasticity; in particular, species belonging to the genus Spongia show different morphs, such as fan-like, digitate, massive or encrusting, that can coexist in the same species (de Laubenfels and Storr, 1958). The genus Spongia inhabits shallow waters in both tropical and temperate regions, even some polar species are known (Vicente, 1989; Sarà et al., 1992). By this study, the different morphofunctional specializations of the external aquiferous system of three species (S. virgultosa (Schmidt, 1868), S. officinalis L., 1759 and S. agaricina Pallas, 1766) have been related to the physical factors influencing both their specializations and distribution along a vertical rocky cliff; in particular hydrodynamic conditions and sedimentation rate. The skeletal network and the foreign materials embed- ded in the sponge body have been taken in account both from a qualitative and a granulometric point of view. MATERIALS AND METHODS The bathymetric distribution of the three species has been studied by SCUBA diving over 1 yr, for a total dive time of 30 h, and recording their presence on the coast of the Portofino Promontory (Punta del Faro, 44°18'N, 9°12'E, Ligurian Sea, Italy). Species densities have been recorded along 10 vertical 1-m wide line-transects from 60 m depth to the surface, following Hiscock’s (1987) method. The deepest observations (to 100 m depth) were conducted with an underwater camera 317 318 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 2, 1998 Figure 1. The three species photographed in situ. a) Spongia virgultosa: i = inhalant funnels; e = exhalant funnels. (Portofino Faro, 5 m depth). b) Spongia officinalis, (Portofino Faro, 15 m depth). c) Spongia agaricina, (Portofino Faro, 45 m depth). (Scale bar = cm). PRONZATO ET AL.: SPONGIA ADAPTATIONS 319 (ROV), during the spring of the sampling year and in the same area for a total time of 10 h. For each species, the maximum diameter of about 50 specimens was recorded in situ. The particular living habitus of S. virgultosa allowed only a general in situ survey, so that 30 surfaces of 400 cm2 have been scraped along a transect from the surface to 60 m depth; about 50 specimens collected in this way were measured in the laboratory. Some physical factors involved in the spatial distribution of benthic organisms in coastal waters have been measured in situ. Using the method of Muus (1968), five groups of plaster balls have been placed along the cliff every 5 m, from 0 to 30 m depth; 24 h later, the difference in weight of the plaster balls that had occured in that lapse of time, provided information on the conditions of water movement in the sampling areas. Along the studied cliffs, sedimentation rates from the surface to 30 m depth have been obtained by positioning three sediment traps (Bavestrello et al., 1991), at three different depths, where each species had their maximum density: 3, 15 and 25 m depth. Samples were collected monthly for 5 mo. Specimens of each investigated species were collected from the areas of maximum density, for study by Scanning Electron Microscopy (SEM). S. virgultosa (Fig. 1A) was collected at 4 m depth, on a vertical cliff exposed to NE; S. officinalis (Fig. 1B) was collected at 12 m depth, on the same cliff; S. agaricina (Fig. 1C) was collected at 40 m depth and it was found exclusively on horizontal or slanted substrates. For SEM analyses, portions of the collected specimens were left to rot in natural sea water for some days and then rinsed in freshwater and dried, following the same method utilized by Greek fishermen to clean commercial sponges. Critical point drying was achieved with a CO2 Pabish CPD 750 apparatus. Thereafter small portions of the skeletal network were mounted on stubs, coated with gold in a Blazers Union evaporator and observed with a Philips 515 SEM. Moreover, to investigate the ultrastructure of the external surface of the three species, samples of each were collected in the same areas described above, directly fixed underwater in 2.5% gluteraldehyde in Gibbons sea water (GSW) and left in this medium for 1 h. For SEM studies, the material was repeatedly rinsed in GSW and dehydrated in graded ethanols. Thereafter the same method for SEM observations described above was used. Both trapped sediments and foreign materials embedded by the sponges were previously exam- ined by dissolving the organic matter in boiling hydrogen peroxide (130 vol.). To evaluate different granulometric distributions of sediments in the sponge bodies, the ectosome, choanosome and iso- lated spongine fibers have been considered separately for each species. Five slides were prepared for each part of the three species and for each sample of trapped sediments; granulometric features of sediments and percentage of spicules were recorded in each slide. The main axis of 200 sand grains was measured using a light microscope with a camera lucida and a GRAPHTEX KD 4300 digitizer connected to an IBM PC. Moreover, a qualitative analysis of the embedded material by a trasmission polarized light micro- scope was conducted to evaluate mineralogical differences between the sediments coming from the external environment and those found on and in the sponge body. RESULTS On the Portofino Promontory the genus Spongia is represented by three species: S. virgultosa, S. officinalis and S. agaricina. Sedimentation rates and water movement intensities (Table 1) revealed a linear dou- bling of the amount of sediments collected by traps from the surface to 25 m depth, and a regular decrease of water movement intensity with depth. DISTRIBUTION AND SHAPE.—S. virgultosa showed an unusual distribution and was found mainly between 3 to 10 m. At deeper levels, it was found in the coralligenous biocoenosis which, in this SE facing site, begins at 20 m depth. The analyses of the standard samples 320 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 2, 1998 Table 1. Bathymetric distribution of aignopS along the coast of Portofino Faro, from 0 to 100 m depth. The variation in population density for each species are indicated. Values of water movement and sedimentation rate along the studied cliff are also reported. Water movement Sedimentation asotlugriv.S S. officinalis S. agaricina Depth (% of surface) (g m2 y−1) (no. m−2) (no. m−2) (no. m−2) 03–10 m 2410.850–1000–0. 1960–20m 10.51–105.5–0–0.00 250–30m08.25.150–105–0.0–0.00 350–50m00. 05–0.30.02–0.0 550–100m00. 00.02–0.05 of 400 cm2 showed the lowest abundance of this species at this depth (Table 1). At the shallowest depth, this species had an average density of about 100 specimens m−2. Whereas at deeper levels its density decreased to about 10–15 specimens m−2. Its average size ranged from 20 to 60 mm for the base diameter, about 10–20 mm for the funnels hight and 3–4 mm for the funnel diameter, both incurrent and excurrent. No variations in shape and size have been found at the various depths. The trend of the bathymetric distribution of S. officinalis showed a maximum density (about 1 m−2 specimens) between 12 and 20 m depth on the SE facing side of the Portofino Promontory (Table 1). The diameters of specimens at these depths ranged from 15 and 25 cm. Specimens were distributed above and below this level too, but were more common at the upper level. Specimens sizes varied with depth and with the different exposure of the cliff. The biggest specimens were found between 3 and 6 m depth on the E-NE facing side of the cliff. Sponges living on the exposed vertical cliff, from the surface to about 3– 5 m depth, were massive; at deeper levels, they assumed a massive-globular shape; in semi-dark caves, they had a white color, a tendency to become columnar and with a minor number of oscula per surface unit. S. agaricina was scattered at the deepest bottoms, nevertheless a notable settlement (density of about 0.005 specimens m−2) was noted on the E-SE facing side of the cliff and exclusively below 15 m depth (Table 1).
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