The non‐hierarchical, non‐uniformly branching topology of a leuconoid sponge aquiferous system revealed by 3D reconstruction and morphometrics using corrosion casting and X‐ray microtomography

Abstract

Hammel, J.U., Filatov, M.V., Herzen, J, Beckmann, F., Kaandorp, J.A. and Nickel M. 2011. The non‐hierarchical, non‐uniformly branching topology of a leuconoid sponge aquiferous system revealed by 3D reconstruction and morphometrics using corrosion casting and X‐ray microtomography. —Acta Zoologica (Stockholm) 00:1–12. As sessile filter feeders, sponges rely on a highly efficient fluid transport system. Their physiology depends on efficient water exchange, which is performed by the aquiferous system. This prominent poriferan anatomical character represents a dense network of incurrent and excurrent canals on which we lack detailed 3D models. To overcome this, we investigated the complex leucon‐type architecture in the demosponge Tethya wilhelma using corrosion casting, microtomography, and 3D reconstructions. Our integrative qualitative and quantitative approach allowed us to create, for the first time, high‐resolution 3D representations of entire canal systems which were used for detailed geometric and morphometric measurements. Canal diameters lack distinct size classes, and bifurcations are non‐uniformly ramified. A relatively high number of bifurcations show previously unknown and atypical cross‐sectional area ratios. Scaling properties and topological patterns of the canals indicate a more complex overall architecture than previously assumed. As a consequence, it might be more convenient to group canals into functional units rather than hierarchical clusters. Our data qualify the leucon canal system architecture of T. wilhelma as a highly efficient fluid transport system adapted toward minimal flow resistance. Our results and approach are relevant for a better understanding of sponge biology and cultivation techniques.

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

“…Research into the biomechanics and fluid dynamics of filter-feeding and into biological fluid transport systems in general has revealed a close interdependence between hydrodynamic constraints, the micro- and macro-morphology of the cellular elements involved and, indeed, the structure of the anatomy in its entirety [1] – [6] . A number of hydrodynamic constraints and optimality principles have been suggested to play a role in shaping the general architecture of the canal system [3] , but the key features appear to be flow resistance and pressure drop [2] .…”

“…The morphometric and anatomical data pertaining to the architecture of the canal system and the cell types involved then needs to be integrated into basic fluid dynamic theory in order to gain a deeper and more detailed understanding of the hydrodynamic situation as a whole in sponge canal systems. Current understanding is based on general information regarding leucon-type canal systems [3] , [4] , [9] , [10] and recent specific morphometric and hierarchical data pertaining to the aquiferous system [6] . Flow velocity within the canal system is affected most prominently by the total available cross-sectional area of every functional unit in it ( Figure 1A–C ) [3] , [4] , [11] .…”

“…However, the cross-sectional area of single segments on a hierarchical level is usually small. Overall increases in cross-sectional area are related to increases in the number of small sized segments on the respective level [6] , [12] . As the lower cross-sectional area of small sized canals is a consequence of their smaller diameter we can draw from the following two equations a direct relationship between pressure drop and resistance: Where R is resistance, η the viscosity of the fluid, l the length of a canal segment, r the canal diameter, ΔP is pressure drop and Q is flow.…”

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

“…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.…”

“…More than 30 years later, this statement is still valid. Even though much advancement were achieved in investigating the three‐dimensional architecture of some species (Bavestrello et al, , ; Hammel et al, ), there are still several questions on the organization and function of the main characteristic of the sponges (Leys & Hill, ). Here, we demonstrated that the investigated specimens of C. caelum were repent, having their oscula aligned at their apical portion of their body.…”