Colonial system of integration and communication pores in a polymorphic bryozoan Dendrobeania fruticosa (Bryozoa: Cheilostomata)

Abstract

Bryozoan colonies are composed of zooids, which can differ in structure and function. Autozooids supply heteromorphic zooids with nutrients, which are usually unable to feed. To date, the ultrastructure of the tissues providing nutrient transfer is almost unexplored. Here, we present a detailed description of the colonial system of integration (CSI) and the different types of pore plates in Dendrobeania fruticosa. All cells of the CSI are joined by tight junctions that isolate its lumen. The lumen of the CSI is not a single structure, but a dense network of small interstices filled with a heterogeneous matrix. In autozooids, the CSI is composed of two types of cells: elongated and stellate. Elongated cells form the central part of the CSI, including two main longitudinal cords and several main branches to the gut and pore plates. Stellate cells compose the peripheral part of the CSI, which is a delicate mesh starting from the central part and reaching various structures of autozooids. Autozooids have two tiny muscular funiculi, which start from the caecum apex and run to the basal wall. Each funiculus includes a central cord of extracellular matrix and two longitudinal muscle cells; together they are enveloped with a layer of cells. The rosette complexes of all types of pore plates in D. fruticosa display a similar cellular composition: a cincture cell and a few special cells; limiting cells are absent. Special cells have bidirectional polarity in interautozooidal and avicularian pore plates. This is probably due to the need for bidirectional transport of nutrients during degeneration–regeneration cycles. Cincture cells and epidermal cells of pore plates contain microtubules and inclusions resembling dense‐cored vesicles, which are typical of neurons. Probably, cincture cells are involved in the signal transduction from one zooid to another and can be a part of the colony‐wide nervous system.

To be a transit link: Similarity in the structure of colonial system of integration and communication pores in autozooids and avicularia of Terminoflustra membranaceotruncata (Bryozoa: Cheilostomata)

“…The caecum is connected to the cystid wall by a funiculus (sometimes termed “primary funiculus” or “caecal ligament”). In all bryozoan groups, the “primary funiculus” has longitudinal muscles; this has been confirmed with both confocal microscopy (Pröts et al, 2019; Schwaha & Wanninger, 2018; Schwaha et al, 2020) and TEM (Carle & Ruppert, 1983; Mukai et al, 1997; Shunatova & Tamberg, 2019; Shunatova et al, 2023; Tamberg et al, 2021). Among phylactolaemates, the funiculus is a unitary structure, and four species studied with TEM ( Fredericella sultana , Plumatella repens , Pectinatella magnifica , and Asajirella gelatinosa ) demonstrate a high similarity in its organization: it is tube‐shaped with a central lumen surrounded by an ECM layer and longitudinal muscles (Carle & Ruppert, 1983; Mukai et al, 1997).…”

“…The presence of several communication pores connecting an avicularium and adjacent autozooids also facilitates the transit of nutrient through avicularium from one autozooid to the next. In contrast, adventitious avicularia of D. fruticosa have a single contact site, that is, a multiporous pore plate, between their CSI and the CSI of a progenitor autozooid (Shunatova et al, 2023). Highly specialized avicularia of D. fruticosa cannot bud off other zooids and represent one of the "end users" of nutrient transport in a colony.…”

“…The inclusions in storage cells of Bugulina flabellata have a different appearance (see Plate V(f) in Dyrynda & King, 1983) compared to other published data. Storage cells are assumed to accumulate nutrients and subsequently release them; these cells are associated with the cystid wall, branches of the CSI ("funicular cords") or developing gametes (Dyrynda & King, 1983;Hughes, 1987;Nekliudova et al, 2019Nekliudova et al, , 2021Shunatova et al, 2023). The pathways of nutrient accumulation and delivery by storage cells (and even the nature of these nutrients) are still unknown.…”

“…Published data on the structure of the CSI are limited. The branching pattern of the CSI in autozooids was studied in Membranipora membranacea (Banta, 1969;Lutaud, 1961), Watersipora nigra (Banta, 1969), E. pilosa (Lutaud, 1982a), and D. fruticosa (Shunatova at al., 2023). The ultrastructure of the CSI in autozooids was described for E. pilosa (Lutaud, 1982a) and was briefly mentioned for Bugula neritina (Carle & Ruppert, 1983) and E. loricata (Shunatova & Tamberg, 2019); in these species, the CSI is composed of a single cell type.…”

“…The ultrastructure of rosette complexes was described for three ctenostomes, Amathia imbricata, Alcyonidium hirsutum (Gordon, 1975), and A. verticillata (Carle & Ruppert, 1983), and two cheilostomes, M. membranacea (Lutaud, 1991) and D. fruticosa (Shunatova et al, 2021(Shunatova et al, , 2023. Nevertheless, only the study of D. fruticosa provides a comparative analysis of different types of pore plates in the same species (Shunatova et al, 2023). We showed that all types of pore plates (transverse and lateral interautozooidal, avicularian, and kenozooidal) display similar cellular composition, although the polarity of special cells in the cluster plugging the communication pore differs: it is unidirectional in kenozooidal pore plates and bidirectional in the interautozooidal and avicularian pore plates.…”