The nervous system of Paludicella articulata - first evidence of a neuroepithelium in a ctenostome ectoproct

Abstract

IntroductionComparatively few data are available concerning the structure of the adult nervous system in the Ectoprocta or Bryozoa. In contrast to all other ectoprocts, the cerebral ganglion of phylactolaemates contains a central fluid-filled lumen surrounded by a neuroepithelium. Preliminary observations have shown a small lumen within the cerebral ganglion of the ctenostome Paludicella articulata. Ctenostome-grade ectoprocts are of phylogenetic relevance since they are considered to have retained ancestral ectoproct features. Therefore, the ctenostome Paludicella articulata was analyzed in order to contribute to the basal neural bauplan of ctenostomes and the Ectoprocta in general.ResultsThe presence of a lumen and a neuroepithelial organization of the nerve cells within the cerebral ganglion are confirmed. Four tentacle nerves project from the cerebral ganglion into each tentacle. Three of the tentacle nerves (one abfrontal and two latero-frontal nerves) have an intertentacular origin, whereas the medio-frontal nerve arises from the cerebral ganglion. Six to eight visceral nerves and four tentacle sheath nerves are found to emanate from the cerebral ganglion and innervate the digestive tract and the tentacle sheath, respectively.ConclusionsThe situation in P. articulata corresponds to the situation found in other ctenostomes and supports the notion that four tentacle nerves are the ancestral configuration in Ectoprocta and not six as proposed earlier. The presence of a lumen in the ganglion represents the ancestral state in Ectoprocta which disappears during ontogeny in all except in adult Phylactolaemata and P. articulata. It appears likely that it has been overlooked in earlier studies owing to its small size.

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

“…It appears tempting to correlate the lack of ciliation in gymnolaemates to the comparatively sparsely innervated body wall. However, care should be taken in this case since peritoneal ciliation has been described in the ctenostome Paludicella articulata (Braem, ; Mukai et al, , see also Weber et al ). In this species, it forms two distinct stripes on the body wall.…”

“…The body wall (cystid) innervation in Hyalinella punctata is similar to other descriptions on phylactolaemates and consists of a regular nerve plexus (Mukai et al, ; Shunkina et al, ). In the ctenostome Paludicella articulata the cystid displayed almost no signal in stainings with antibodies against acetylated α‐tubulin (Weber et al, ), whereas paired cystidial nerves were encountered by stainings of serotonin‐like immunoreactivity (Schwaha & Wanninger, ). The diffuse innervation pattern of the Phylactolaemata corresponds to the regular arrangement of body wall musculature (Mukai et al, ; Schwaha & Wanninger, ).…”

“…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.…”

“…In another cheilostome species with four neurite bundles located subepidermally ( Cryptosula pallasiana ), two additional subperitoneally neurites have been described (Gordon, ). Subperitoneal structures/cells have been described for all major bryozoan classes, but their definite characterization as neuronal structures remains questionable (see Weber et al, ).…”

“…The bryozoan nervous system has been subject of several studies (see Gruhl & Schwaha, for review), but only few have employed modern techniques such as immunocytochemistry and confocal laser scanning microscopy on larval (e.g., Gruhl, ; Santagata, ; Schwaha, Handschuh, Redl, & Wanninger, Shimizu, Hunter, & Fusetani, ) or adults of this phylum (Schwaha, Wood, & Wanninger, ; Schwaha & Wanninger, ; Shunkina et al, ; Temereva & Kosevich, ; Weber, Wanninger, & Schwaha, ). A recent study investigated the nervous system in three phylactolaemates with modern techniques (Shunkina et al, ).…”