Organogenesis during budding and lophophoral morphology of Hislopia malayensis Annandale, 1916 (Bryozoa, Ctenostomata)

Abstract

BackgroundBryozoans represent a large lophotrochozoan phylum with controversially discussed phylogenetic position and in group relationships. Developmental processes during the budding of bryozoans are in need for revision. Just recently a study on a phylactolaemate bryozoan gave a comprehensive basis for further comparisons among bryozoans. The aim of this study is to gain more insight into developmental patterns during polypide formation in the budding process of bryozoans. Particular focus is laid upon the lophophore, also its condition in adults. For this purpose we studied organogenesis during budding and lophophoral morphology of the ctenostome bryozoan Hislopia malayensis.ResultsPolypide buds develop on the frontal side of the developing cystid as proliferation of the epidermal and peritoneal layer. Early buds develop a lumen bordered by the inner budding layer resulting in the shape of a two-layered sac or vesicle. The hind- and midgut anlagen are first to develop as outpocketing of the prospective anal area. These grow towards the prospective mouth area where a comparatively small invagination marks the formation of the foregut. In between the prospective mouth and anus the ganglion develops as an invagination protruding in between the developing gut loop. Lophophore development starts with two lateral ridges which form tentacles very early. At the lophophoral base, intertentacular pits, previously unknown for ctenostomes, develop. The ganglion develops a circum-oral nerve ring from which the tentacle nerves branch off in adult zooids. Tentacles are innervated by medio-frontal nerves arising directly from the nerve ring, and medio-frontal and abfrontal nerves which originate both from an intertentacular fork.ConclusionsWe are able to show distinct similarities among bryozoans in the formation of the different organ systems: a two-layered vesicle-like early bud, the ganglion forming as an invagination of the epidermal layer in between the prospective mouth and anal area, the digestive tract mainly forming as an outpocketing of the prospective anal area, and the lophophore forming from two lateral anlagen that first fuse on the oral and afterwards on the anal side. Future studies will concentrate on cyclostome budding to complement our knowledge on developmental patterns of bryozoans.

Organization and metamorphic remodeling of the nervous system in juveniles of Phoronopsis harmeri (Phoronida): insights into evolution of the bilaterian nervous system

“…The same intertentacular branches are known in adult bryozoans [43,44]. They originate from the circum-oral nerve ring that arises from the cerebral ganglion.…”

Body cavities in bryozoans: Functional and phylogenetic implications

“…Unfortunately, data about the zooid formation in gymnolaemates both during budding and metamorphosis are scarce. Polypide organogenesis during budding was described at the light microscopy level for two ctenostome species: Paludicella articulata (Davenport, ) and Hislopia malayensis (Schwaha & Wood, ). Lutaud (, ) provided some ultrastructural data on the formation of the peritoneal lining around the gut and tentacle sheath during polypide development in two cheilostome species ( Membranipora membranacea and E. pilosa ).…”

Neuroanatomy of Hyalinella punctata: Common patterns and new characters in phylactolaemate bryozoans

“…Because the cerebral ganglion develops from an invagination of the prospective pharynx epithelium, it has a vesicle‐like appearance in early development and bears a fluid‐filled cavity in all bryozoan species investigated to date (Braem, ; Davenport, ; Graupner, ; Nitsche, ). In almost all studied stenolaemates and gymnolaemates the lumen disappears during ontogeny (Borg, ; Schwaha & Wood, ). Only recently, two ctenostome gymnolaemates were found to possess a lumen or small cleft within the cerebral ganglion, thus reflecting the condition found in the Phylactolaemata (Temereva & Kosevich, ; Weber et al, ).…”

“…While the medio‐frontal neurite bundle branches off from the cerebral ganglion, respectively from the circum‐oral nerve ring itself, the other tentacle neurite bundles have an intertentacular origin. In several ctenostomes four tentacle neurite bundles were found in each tentacle (Schwaha & Wood, ; Smith, ; Weber et al, ). In the ctenostome Amathia gracilis only, the tentacles are innervated by two neurite bundles, one frontally and one abfrontally.…”