Detailed morphology of tentacular apparatus and central nervous system in Owenia borealis (Annelida, Oweniidae)

Abstract

The Oweniidae are marine annelids with many unusual features of organ system, development, morphology, and ultrastructure. Together with magelonids, oweniids have been placed within the Palaeoannelida, a sister group to all remaining annelids. The study of this group may increase our understanding of the early evolution of annelids (including their radiation and diversification). In the current research, the morphology and ulta-anatomy of the head region of Owenia borealis is studied by scanning electron microscopy (SEM), 3D reconstructions, transmission electron microscopy (TEM), and whole-mount immunostaining with confocal laser scanning microscopy. According to SEM, the tentacle apparatus consists of 8–14 branched arms, which are covered by monociliary cells that form a ciliary groove extending along the oral side of the arm base. Each tentacle contains a coelomic cavity with a network of blood capillaries. Monociliary myoepithelial cells of the tentacle coelomic cavity form both the longitudinal and the transverse muscles. The structure of this myoepithelium is intermediate between a simple and pseudo-stratified myoepithelium. Overall, tentacles lack prominent zonality, i.e., co-localization of ciliary zones, neurite bundles, and muscles. This organization, which indicates a non-specialized tentacle crown in O. borealis and other oweniids with tentacles, may be ancestral for annelids. TEM, light, and confocal laser scanning microscopy revealed that the head region contains the anterior nerve center comprising of outer and inner (=circumoral) nerve rings. Both nerve rings are organized as concentrated nerve plexus, which contains perikarya and neurites extending between basal projections of epithelial cells (radial glia). The outer nerve ring gives rise to several thick neurite bundles, which branch and extend along aboral side of each tentacle. Accordingly to their immunoreactivity, both rings of the anterior nerve center could be homologized with the dorsal roots of circumesophageal connectives of the typical annelids. Accordingly to its ultrastructure, the outer nerve ring of O. borealis and so-called brain of other oweniids can not be regarded as a typical brain, i.e. the most anterior ganglion, because it lacks ganglionic structure.

First Immunodetection of Sensory and Nervous Systems of Parasitic Larvae (Glochidia) of Freshwater Bivalve Nodularia douglasiae

“…Acetylation of alpha-tubulin is widely used to detect ciliary structures in annelid, mollusk, and nemertine larvae ( Wanninger, 2015 ; Yurchenko et al, 2019 ; Magarlamov et al, 2020 ). In addition, these antibodies mark neuronal elements in some adult mollusks and annelids ( Faller et al, 2012 ; Kotsyuba et al, 2020 ; Temereva et al, 2021 ). Therefore, mollusk larvae stained only with secondary antibodies were analyzed as controls for all primary antibodies.…”

Ultrastructure of proboscis blood vessels in females of Bonellia viridis (Annelida: Bonellinae): New reconstructions

“…An exact study of serial sections of the whole vessel allowed us to discover adherence junctions between cells, borders between cells, and that myofilaments are present in all myoepithelial cells, but not in certain areas of the axial vessel (Figure 3). Our study revealed that the ultrastructure of the wall of the axial and lateral vessels of B. viridis corresponds to a simple type of coelothelium, which is known in many annelids (Bartolomaeus, 1994;Fransen, 1988;Gardiner, 1992;Rieger, 1980;Temereva et al, 2021) and other bilaterians (Kuzmina et al, 2018;Rieger & Lombardi, 1987;Temereva, 2015Temereva, , 2017. The great difference between B. viridis axial vessels and blood vessels of other coelomic bilaterians is the absence of a coelomic canal around the axial vessel.…”

“…The histological organization of proboscis blood vessels is simple: it consists of a layer of basal lamina and lacks the endothelial lining. Such a structure can be compared with blood capillaries of some other bilaterians (Kuzmina et al, 2018; Temereva & Malakhov, 2004; Temereva et al, 2021).…”

“…Such a structure can be compared with blood capillaries of some other bilaterians (Kuzmina et al, 2018;Temereva & Malakhov, 2004;Temereva et al, 2021).…”

Loss of nervous system complexity – Morphological analyses shed light on the neuronal evolution in Myzostomida (Annelida)

“…Interestingly, nuchal organs and complex cup‐shaped eyes are also absent in adult specimens (Helm et al, 2022). Comparable patterns are also observable for members of the Palaeoannelida, namely the Oweniidae and Magelonidae (Beckers et al, 2019; Helm et al, 2016; Rimskaya‐Korsakova et al, 2016; Temereva et al, 2021). In all these cases observed so far, a change of lifestyle from planktonic towards sedentary is linked with a significant reduction of neuronal complexity.…”