Respiration kinetics and allometric scaling in the demosponge Halichondria panicea

Abstract

Background: The aquiferous system in sponges represents one of the simplest circulatory systems used by animals for the internal uptake and distribution of oxygen and metabolic substrates. Its modular organization enables sponges to metabolically scale with size differently than animals with an internal circulatory system. In this case, metabolic rate is typically limited by surface to volume constraints to maintain an efficient supply of oxygen and food. Here, we consider the linkeage between oxygen concentration, the respiration rates of sponges and sponge size.

Results: We explored respiration kinetics for individuals of the demosponge Halichondria panicea with varying numbers of aquiferous modules (n_modules = 1-102). From this work we establish relationships between the sponge size, module number, maximum respiration rate (R_max) and the half-saturation constant, K_m, which is the oxygen concentration producing half of the maximum respiration rate, R_max. We found that the n_modules in H. panicea scales consistently with sponge volume (V_sp) and that R_max increased with sponge size with a proportionality > 1. Conversly, we found a lack of correlation between K_m and sponge body size suggesting that oxygen concentration does not control the size of sponges.

Conclusions: The present study reveals that the addition of aquiferous modules (with a mean volume of 1.59 ± 0.22 mL) enables H. panicea in particular, and likely demosponges in general, to grow far beyond constraints limiting the size of their component modules and independent of ambient oxygen levels.

Keywords: Animal evolution; Metabolic scaling; Modularity; Oxygen; Respiration kinetics; Sponges.

Fig. 1

Left panel: Multi-oscula Halichondria panicea specimen (A) on a PVC net (B) in respiration chamber with well-mixed seawater (T = 12.4 ± 0.1 °C, S = 20 PSU). Each osculum (indicated by the white arrow) corresponds to an aquiferous module, representing a specific volume in the sponge that is supplied by an internal system of water canals [24, 25]. Right panel: Respiration chambers with (C) and without sponge (= control, D) were submerged in a temperature-controlled water-bath (E) to minimize temperature variations during measurements of the dissolved oxygen (DO, % AS) in respiration chambers. Optical fibers were attached to a contactless oxygen sensor spot glued to the inner wall of the chamber lid (F) to monitor the DO using FireStingO₂ optical oxygen meter (PyroScience, Germany)

Fig. 2

A Example of oxygen (% AS) drawdown recorded in respiration chamber with (ID1, dark line) and without a sponge (i.e. control, grey line). B Dry weight-specific respiration rate (R_DW, µmol O₂ h⁻¹ g (DW)⁻¹) of a sponge (ID1) plotted as a function of dissolved oxygen (DO, % AS) in seawater. Open circles indicate outliers which were not considered for determinations of the maximum R_DW and the half-saturation constant K_m (% AS) (Additional file 1: Figures S1, S2). Line represents model fit

Fig. 3

Relationship between the number of modules (n_modules) and sponge volume (V_sp, cm³) plotted on a double logarithmic scale

Fig. 4

Maximum respiration rate (R, µmol O₂ h⁻¹) as a function of A) the sponge dry weight (DW, g), B) volume (V_sp, cm³), C) number of modules (n_modules) and D) module volume (V_module, cm³) plotted on a double logarithmic scale. Regression line (dark line) and equation of the fitted power function is shown

Fig. 5

Half-saturation constant (K_m, % AS) as a function of sponge size, i.e. A) sponge dry weight (DW, g), B) sponge volume (V_sp, cm³), C) number of modules (n_modules), and D) module volume (V_module, cm³). Error bars represent the standard error (SE) of the model fit

Fig. 6

Compilation of half-saturation constants (K_m, % AS) for respiration of various aerobic unicellular organisms and organelles (left) and multicellular organisms (right) as a function of their linear dimensions, plotted on a double logarithmic scale. Closed points represent data taken from ([2], and references therein), including crustaceans (1–4, 6, 8–9), fish (5,7), the annelid worm Tubifex (10), ciliates (11,12), the amoeba Acanthamoeba (13), yeast (14), and Tubifex mitochondria (15). Closed square shows mean K_m for several (n = 13) multi-oscula H. panicea sponges varying in size. Bars indicate standard deviations. Open squares in separate plot show K_m of H. panicea individuals investigated in the present study. Dotted regression line is shown