A New Flow-Regulating Cell Type in the Demosponge Tethya wilhelma – Functional Cellular Anatomy of a Leuconoid Canal System

Abstract

Demosponges possess a leucon-type canal system which is characterized by a highly complex network of canal segments and choanocyte chambers. As sponges are sessile filter feeders, their aquiferous system plays an essential role in various fundamental physiological processes. Due to the morphological and architectural complexity of the canal system and the strong interdependence between flow conditions and anatomy, our understanding of fluid dynamics throughout leuconoid systems is patchy. This paper provides comprehensive morphometric data on the general architecture of the canal system, flow measurements and detailed cellular anatomical information to help fill in the gaps. We focus on the functional cellular anatomy of the aquiferous system and discuss all relevant cell types in the context of hydrodynamic and evolutionary constraints. Our analysis is based on the canal system of the tropical demosponge Tethya wilhelma, which we studied using scanning electron microscopy. We found a hitherto undescribed cell type, the reticuloapopylocyte, which is involved in flow regulation in the choanocyte chambers. It has a highly fenestrated, grid-like morphology and covers the apopylar opening. The minute opening of the reticuloapopylocyte occurs in an opened, intermediate and closed state. These states permit a gradual regulation of the total apopylar opening area. In this paper the three states are included in a theoretical study into flow conditions which aims to draw a link between functional cellular anatomy, the hydrodynamic situation and the regular body contractions seen in T. wilhelma. This provides a basis for new hypotheses regarding the function of bypass elements and the role of hydrostatic pressure in body contractions. Our study provides insights into the local and global flow conditions in the sponge canal system and thus enhances current understanding of related physiological processes.

Profiling cellular diversity in sponges informs animal cell type and nervous system evolution

“…3A and fig. S1M-N), and are thought to regulate water currents inside of the sponge via control of the diameter of the efflux opening (22). We also discovered myopeptidocytes, an abundant yet previously undescribed constituent of the mesohyl (Fig.…”

Using a thermistor flowmeter with attached video camera for monitoring sponge excurrent speed and oscular behaviour

“…According to Ludeman et al (2014), the osculum itself may now be considered a sensory organ that coordinates behavioural responses, sensing and reacting to decreased pumping by choanocytes. Flow sensing ciliated pinacocytes have been identified in oscula from numerous sponge species and classes (Hammel & Nickel, 2014; Ludeman et al, 2014). Although flow sensing cilia structures have not yet been observed in C. orientalis , it is likely that they are present given our results.…”

Anatomy and ultrastructure of the tropical sponge Cladocroce caelum (Haplosclerida, Demospongiae)

“…and Haliclona elegans (Langenbruch & Scalera‐Liaci, ). It is hypothesized that apopylar cells and prosopyles can contract and relax to control the water flow in the aquiferous system (De Vos et al, 1990; Hammel & Nickel, ; Reiswig, ). In sponges with pinacocytic prosopyles and/or porocytes the entrance of water into the chambers can be easily controlled by closing these openings.…”

“…The caliber of the holes and valves along the water path of the sponge is an important characteristic to understand how the water flows through the canals and chambers of the aquiferous system of the sponges (Hammel & Nickel, ; Ludeman et al, ; Reiswig, ). Besides being important to comprehend the velocity of water movement and the energetic cost for the filtering activity, the diameter of the opening in the aquiferous system may indicate the feeding habit of the sponge.…”

“…Larger particles (such as yeasts, flagellates, and other small eukaryotes) are possibly retained along the inhalant and exhalant canals or by the outer surface of the choanocyte chambers, while bacteria are likely entrapped by the choanocytes (Langenbruch, ; Weissenfels, , ; Willenz, ; Willenz & Van de Vyver, ). In addition, some of these larger particles may not be engulfed in the canals, exiting the body of the sponge possibly by bypasses in the aquiferous system (Bavestrello, Arillo, Calcinai, & Cerrano, ; Bavestrello, Calcinai, Boyer, Cerrano, & Pansini, ; Hammel et al, ; Hammel & Nickel, ; Ludeman et al, ). It will be important to investigate the architecture of the aquiferous system of this species either using corrosion casts (e.g., Bavestrello et al, ), micro CT‐Scanning (Hammel et al, ), or by 3D reconstruction from serial sections (e.g., Brenzinger, Padula, & Schrödl, ; Leys, Zaman, & Boury‐Esnault, ) to better comprehend the water path in this species.…”