The Gutless Marine Oligochaete Phallodrilus leukodermatus. Structural Studies on an Aberrant Tubificid Associated with Bacteria

Abstract

Studies on anatomy and ultrastructure of the gutless tubificid Phallodrilus leukodermatus (Oligochaeta, Annelida) revealed the complete absence of intestinal tissues. However the w~d e , septate coelornic cavity is traversed by alveolate (mesodermal?) cells between which are embedded few longitudinal or oblique muscle strands and some blood vessels. The much wrinkled cuticle is densely stud with 'epicuticular projections' (Richards, 1977). In a space system between epidermis and cuticle, particularly wide in the postclitellar region, many gram-negative, rod-shaped bacteria are found. In the posterior part of the worms' body numerous large, multivesiculate, membrane-bound corpuscles which lack typical cell organelles, fill the extra-epidermal subcuticular cavities. It is speculated that the bacteria, found in every specimen examined, are of nutritional significance for the worms. The aberrant anatomy of the tubificids, their association with procaryotes and parallels to other gutless marine animals are discussed.

Morphology and fine structure of two marine tubificids (Oligochaeta), closely related to the gutlessPhallodrilus spp.

“…Their irregular wavy fibres, running mainly in a circular direction, bear more resemblance with the cuticle in the naidid Dero obtusata (Krall, 1968). In this pattern they contrast to the gutless Phallodrilus species (Giere, 1981;Richards, Fleming & Jamieson, 1982) which show an orthogonal collagen grid. This difference within families and even within one genus of interstitially living worms renders generalization or relation of these cuticular structures to life habits problematical (Richards, 1977;Westheide & Rieger, 1978).…”

“…The endothelial ceils, too, have attained a different appearance in the gutless coelome: they seem 'blown up' and, in some sections, fill the whole cavity almost resembling a fluffy O. Giere mesenchyma (Fig. 1 in Giere, 1981). Their rich content of endoplasmatic reticulum, lined by ribosomes, mitochondria, electron-dense grana, however, functionally resembles normal chloragocytes (see above).…”

“…Both Tubifex tubifex (Fischer & Horv~th, 1977) and the gutless relatives have shorter and simple epicuticular projections which lack any brush-like tips (Giere, 1981;Richards et al, 1982). This leaves room for spe~ation on the function of these structures, whether as means for the transepidermal uptake of nutrients or, as suggested by Richards et al, (1982), for mere protection.…”

“…In P. Ieukodermatus (Giere, 1981), the most striking difference, the complete absence of gut and nephridia, has apparently marked consequences for the struchlre of the vascular system and chloragocytes: while in the 'normal' worms the vessels are via the chloragogenic tissue in loose connection with the intestine and nerve cord, in the anenteric form the two large longitudinal vessels, connected by a muscular strand, traverse more or less freely the 'empty' coelomic cavity. Hence, any homology for a ventral or dorsal vessel is here problematical.…”

“…In a special research project, the gutless oligochaete Phallodrilus leukodermatus from Bermuda is the subject of thorough examination (Giere, 1979(Giere, , 1981Giere et al, 1982Giere et al, , 1983. This species has, in contrast to the anenteric Pogonophora, close relatives which possess a regular digestive and excretory system.…”