Morphology of the bryozoan Cinctipora elegans (Cyclostomata, Cinctiporidae) with first data on its sexual reproduction and the cyclostome neuro-muscular system

Abstract

BackgroundCyclostome bryozoans are an ancient group of marine colonial suspension-feeders comprising approximately 700 extant species. Previous morphological studies are mainly restricted to skeletal characters whereas data on soft tissues obtained by state-of-the-art methods are still lacking. In order to contribute to issues related to cyclostome ground pattern reconstruction, we analyzed the morphology of the neuromuscular system Cinctipora elegans by means of immunocytochemical staining, confocal laser scanning microscopy, histological sections and microCT imaging.ResultsPolypides of C. elegans are located in elongated tubular skeletal cystids. Distally, the orifice leads into a prominent vestibulum which is lined by an epithelium that joins an almost complete perimetrical attachment organ, both containing radially arranged neurite bundles and muscles. Centrally, the prominent atrial sphincter separates the vestibulum from the atrium. The latter is enclosed by the tentacle sheath which contains few longitudinal muscle fibers and two principal neurite bundles. These emerge from the cerebral ganglion, which is located at the lophophoral base. Lateral ganglia are located next to the cerebral ganglion from which the visceral neurite bundles emerge that extend proximally towards the foregut. There are four tentacle neurite bundles that emerge from the ganglia and the circum-oral nerve ring, which encompasses the pharynx. The tentacles possess two striated longitudinal muscles. Short buccal dilatators are situated at the lophophoral base and short muscular sets are present at the abfrontal and frontal side of the tentacle base. The pharynx is myoepithelial and triradiate in cross-section. Oocytes are found inside the pharyngeal myoepithelium. The digestive tract contains dense circular musculature and few longitudinal muscles. The membranous sac contains regular, thin, circular and diagonal muscles and neurites in its epithelial lining.ConclusionsThe general structure of the neuro-muscular system is more reminiscent of the condition found in Gymnolaemata rather than Phylactolaemata, which supports a close relationship between Cyclostomata and Gymnolaemata. Several characters of C. elegans such as the lateral ganglia or loss of the cardia are probably apomorphic for this species. For the first time, oocytes that surprisingly develop in the pharyngeal wall are reported for this species.

The neuromuscular system of the cyclostome bryozoan Crisia eburnea (Linnaeus, 1758)

“…The putative neural, methylene blue staining plexus observed in Crisidia by Lutaud () was not detected with our methods, and it has neither been observed in Cinctipora (Schwaha et al, ) nor in any of the eurystomes studied with immunohistochemistry.…”

“…The retractor muscles seem striated, contrasting Nielsen and Pedersen () who described the muscles as smooth though their figure 22 indicates a striation, albeit not the typical striation with distinct Z‐ and M‐bands seen in the muscle cells of the pharynx. The subtentacular muscles have not been reported in Crisia before but recently in Cinctipora as lophophoral base muscles (Schwaha et al, ). The cross section of the myoepithelial pharynx illustrated in Nielsen (, fig.…”

“…The first descriptions of the soft parts of C. elegans (Boardman, ; Boardman et al, ) were based on traditional light microscopy, whereas the recent study by Schwaha et al () has used both traditional light microscopy and immunofluorescence combined with confocal laser scanning microscopy, which gives a much higher resolution, especially of the nerves. Scattered information on musculature in other genera can be found in Boardman () and Schäfer ().…”

“…The ectodermal longitudinal muscles of Crisia , which originate at the body wall or at the upper area of the membranous sac and extend in fine branches to their attachment sites at the terminal membrane, are not found in Cinctipora (Schwaha et al, ), which is probably related to the cystid structure, where Crisi a is fixed‐walled and Cinctipora free‐walled.…”

“…Traditional, light microscopy and TEM studies have shown important differences in general structure between the extant cyclostomes and eurystomes, especially in the body wall and the muscles associated with protrusion of the polypide, but the scant knowledge of the cyclostome nervous system has been insufficient for comparative studies. The recent study of C. elegans (Schwaha et al, ), which has unusually large zooids with up to 17 tentacles versus the usual number of 8–12, has provided detailed new information about the neuromuscular system. The present study uses immunostaining of muscles and nerves to complement previous studies of the otherwise well‐studied C. eburnea and now describes the neuromuscular system in details.…”