Video and Electron Microscopy of Particle Feeding in Sandwich Cultures of the Hexactinellid Sponge, Rhabdocalyptus dawsoni

Abstract

Cultured fragments of the hexactinellid sponge, Rhabdocalyptus dawsoni, were observed feeding on 1.0 Jm latex beads. Using contrast-enhanced video microscopy of live cultures, the events preceding, during, and after phagocytosis were observed. Particle ingestion occurred almost exclusively in flagellated areas where the water currents generated by the flagella of collar bodies could trap and hold particles against sponge tissue. Transmission electron microscopy of cultures fixed after feeding on latex beads showed that collar bodies themselves do not participate in particle phagocytosis. Rather, it is the primary and, probably, the secondary reticula of the trabecular reticulum in the flagellated chamber wall which effect phagocytosis. The intact sponge's tissue organization appears admirably suited for particle capture, and these sponges are likely to be, at least in part, particle feeders in their natural habitat. Additional key words: Hexactinellida, Porifera, filter feeding, culture The Hexactinellida (Porifera, subphylum Symplasma) is an enigmatic marine sponge group which has received little attention in the past due to their seclusion in deep waters. However, recent advances exploiting the few shallow-water species available for study have begun to reveal various aspects of their tissue organization, cell biology, and feeding (e.g. Reiswig & Mehl 1991; Boury-Esnault & Vacelet 1994; Leys 1995; Leys & Mackie 1997). Feeding studies have been pursued using two species: Oopsacas minuta TOPSENT 1927, a Mediterranean cave species (Perez 1996), and Rhabdocalyptus dawsoni (LAMBE 1892) a Northeast Pacific fjord species (Wyeth et al. 1996). Investigation of sponge feeding has focused on demosponges (Porifera, subphylum Cellularia), which has established them as non-specific particle feeders. Particles are extracted from water pumped through the body wall by choanocytes. Most tissues of the demosponge body wall have been implicated in particle phagocytosis. In addition to choanocytes, whose collar microvilli strain the current driven by the flagella, exopinacocytes of the dermal surface and endopinacocytes of the incurrent canals have been shown to engulf particles (Schmidt 1970; Diaz 1979; Willenz & Van de Vyver 1982; Imsiecke 1993). Furthermore, investigations of pumping rates (e.g., Reiswig 1971), a E-mail: rwyeth@u.washington.edu feeding and clearance efficiencies (e.g., Reiswig 1975a; Frost 1980), and the demosponge pump design (Larsen & Riisg'ard 1994) have also been conducted. The assumption that hexactinellid and demosponge feeding are the same should not be made a priori, since the two groups differ in the details of tissue organization and structure. In hexactinellids, the dermal membrane, trabeculae of the body wall, and flagellated chamber walls are all formed by the syncytial trabecular reticulum (Mackie & Singla 1983; Reiswig & Mehl 1991; Leys 1999). The hexactinellid aquiferous system consists of broad, expansive incurrent and excurrent canals bounded by a network of trabeculae (Schulze 1887; Ijima 1904; Leys 1999), unlike the smaller diameter canals, bounded by endopinacocytes, found in the demosponges used for feeding studies (Schmidt 1970; Diaz 1979; Imsiecke 1993). The large and oblong hexactinellid flagellated chambers, 60 (Jm or more in maximal dimension, are serviced by proportionately far more prosopyles (Schulze 1887; Ijima 1904; Reiswig & Mehl 1991; Leys 1999) than the smaller (30 Im in diameter) spherical chambers in demosponges used in feeding studies (Reiswig 1975b; Diaz 1979; de Vos et al. 1991). In hexactinellids, the trabecular reticulum branches to create a double reticulum in the chamber wall. The primary reticulum forms the wall of the chamber and encloses the bases of collar bodies. Inside the chamber, the secondary reticulum, offset from the primary, fills the gaps between This content downloaded from 207.46.13.176 on Mon, 20 Jun 2016 07:22:20 UTC All use subject to http://about.jstor.org/terms Hexactinellid sponge feeding collars inside the chamber (Reiswig 1979; Reiswig & Mehl 1991; Boury-Esnault & Vacelet 1994; Leys 1999). Hexactinellid collar bodies, although bearing similar collars of microvilli, are more widely spaced than demosponge choanocytes, are enucleate, and form part of a partially connected network within the flagellated chamber walls (Reiswig 1979; Mackie & Singla 1983; Leys 1999). Furthermore, the 20 tim flagella in hexactinellids are roughly 2-3 times the length of their associated collars (Reiswig 1979; Reiswig & Mehl 1991; Boury-Esnault & Vacelet 1994), considerably smaller than the equivalent ratio in demosponges which may have 45 pLm flagella, 4-6 times the collar length (see Larsen & Riisgard 1994). Although individually none of these structural differences leaps out as a reason to suspect substantial differences between hexactinellid and demosponge feeding, when considered together it is quite possible they could lead to considerable differences in the details of feeding