Endobionts of the Coral Reef Sponge Theonella swinhoei (Porifera, Demospongiae)

Endobionts associated with the coral reef sponge Theonella swinhoei (Lithistida, Demospongiae), from the Red Sea and Indian Ocean, were characterized through histological and ultrastructural investigations. Prokaryotes included unicellular heterotrophic bacteria (mean concentration, 20% of the sponge tissue), unicellular cyanobacteria (Aphanocapsa feldmanni, 15% of the sponge tissue), and non-photosynthetic filamentous forms, probably in the Beggiatoa-group (sulfur bacteria, family Beggiatoaceae, 40% of the sponge tissue). Evidence of ingestion of small pieces of filamentous bacteria by sponge cells was observed. The worm Haplosyllis spongicola (Syllidae, Polychaeta) inhabited the canals of the sponge aquiferous system (mean density, 73 worms/cm3). The abundance and distribution of the endobionts living in T. swinhoei from different localities are presented and discussed in comparison with those of other sponge species reported in literature. Additional key words: polychaetes, filamentous bacteria, cyanobacteria Sponges present an astonishing landscape of associations with various kinds of autotrophic and heterotrophic organisms (Pearse 1932; Pansini 1970; Ilan et al. 1994). The various parts of a sponge, especially the endosome, contain large populations of extracellular bacteria (Vacelet 1975; Vacelet & Donadey 1977), which may greatly differ from the bacterial population in the water surrounding the same sponge (Wilkinson 1978b). The presence of cyanobacteria or other photosynthetic organisms is less frequent. Even though the autotrophic organisms inhabit the more superficial layers in order to fulfill their metabolic needs, some peculiar localizations inside the skeletal fibers (Riitzler 1990) and along the siliceous spicule bundles (Gaino & Sara 1994) have been observed. In this last condition, siliceous spicules, acting as a light-conducting system (Cattaneo-Vietti et al. 1996), enhance photosynthesis. Since the first observations of Feldmann (1933), many ultrastructural studies have stressed the presence of cyanobacteria in sponges of both Mediterranean and tropical origin (Sara 1971; Vacelet 1971; Vacelet & Donadey 1977; Wilkinson 1978a,c; Rutzler 1990). In some cases symbionts are so tightly associated with the sponge tissues as to constitute a "symbiocortex" (Simpson 1984, pp. 114-123). Cyanobacteria protect a Author for correspondence. E-mail: zoologia@unige.it sponges from excessive solar radiation (Sara & Vacelet 1973; Wilkinson 1980) and variations in the photosynthetic symbiont concentration may effect changes in the color of the sponge surface (Gaino et al. 1977). Direct feeding on cyanobacteria has been frequently suggested but observed only for unicellular types (Sara 1966; Wilkinson 1980; Berthold et al. 1982; Rutzler 1990). The translocation of glycerol, fixed nitrogen, and other photosynthetically fixed nutrients represents a trophic advantage for the sponge host (Wilkinson 1979; Wilkinson & Fay 1979), mainly in coral reefs and other tropical environments where the low levels of available nutrients favor these associations (Wilkinson 1987). So far, only two species of unicellular cyanobacteria have been frequently described in association with sponges: Aphanocapsa feldmanni and A. raspaigellae (Sara 1966; Gaino et al. 1976; Wilkinson 1980; Rutzler 1990). A few reports treat filamentous multicellular cyanobacteria, differing in dimension and shape, most commonly Oscillatoria spongeliae (Sara 1966) and Phormidium spongeliae (Wilkinson 1980). Nonetheless, Bewley et al. (1996), in ultrastructural observations, reported the lack of a photosynthetic system in some prokaryotic filaments, previously attributed to the above mentioned cyanobacteria. In addition, sponges serve as hosts to a number of other heterotrophic organisms, providing food and shelter to species from many taxa. Polychaetes have This content downloaded from 157.55.39.153 on Mon, 19 Sep 2016 04:41:51 UTC All use subject to http://about.jstor.org/terms Magnino, Sara, Lancioni, & Gaino been commonly observed in sponges (Pearse 1950; Pawlik 1983; Koukouras et al. 1996; Martin 1996; Rutzler, 1997). In particular, the polychaete Haplosyllis spongicola (GRUBE 1855), family Syllidae, is an abundant inhabitant of sponges. Fauchald & Jumars (1979) proposed that this worm grazes on the sponge surface. A more intimate relationship with its host has been directly observed by Tsurumi & Reiswig (1997), who reported that H. spongicola feeds on the tissues surrounding the sponge water canals, within which it lives. It is often difficult to establish the correct relationship between sponges and their endobionts. The sponge Theonella swinhoei GRAY 1868 (order Lithistida) is a remarkable component of the sponge populations in coral reef communities. Heterospecific associations, representing many types of adaptive interactions, are very common in this peculiar environment (Wilkinson 1987; Castro 1988). Previous studies on T. swinhoei from the Red Sea showed the unicellular symbionts A. feldmanni associated with sponge tissues (Wilkinson 1979, 1980; Bewley et al. 1996). Here we document that specimens of T. swinhoei, from both Red Sea and Indian Ocean coral reefs, constitute a further example of how sponges may represent a suitable micro-environment for the development of various kinds of autotrophic and heterotrophic organisms, which inhabit different parts of the sponge body.