Pumping Rate and Size of Demosponges—Towards an Understanding Using Modeling

Filter-feeding sponges pump large amounts of water and contribute significantly to grazing impact, matter transport and nutrient cycling in many marine benthic communities. For ecological studies it is therefore of interest to be able to estimate the pumping rate of different species from their volume size or osculum cross-sectional area by means of experimentally determined allometric correlations. To help understand allometric data correlations and observed large variations of volume-specific pumping rate among species we developed a model that determines the pumping rate as a function of the size (volume) of a tubular-type demosponge described by 4 geometric length scales. The model relies on a choanocyte-pump model and standard pressure loss relations for flow through the aquiferous system, and density and pumping rate per choanocyte is assumed to be constant. By selecting different possibilities for increase of the length scales, which may also simulate different growth forms, we demonstrate that the model can imitate the experimental allometric correlations. It is concluded that the observed dependence of pumping rate on size is primarily governed by the hydraulics of pump performance and pressure losses of the aquiferous system rather than, e.g., decreasing density of choanocytes with increasing sponge size.

Differences in the Structural Components Influence the Pumping Capacity of Marine Sponges

Marine sponges are important sessile, benthic filter feeders with a body plan designed to pump water efficiently. The sponge body plan generally consists of mineral spicules, gelatinous mesohyl, and the pores and canals of the aquiferous system. These structural components have stark differences in compressibility, mass, and volume; therefore, their proportion and distribution are likely to affect sponge morphology, anatomy, contraction, and finally the pumping capacity. We examined seven demosponge species (from high spicule skeleton contents to no spicules) commonly found along the central west coast of India for structural components, such as total inorganic contents (spicule skeleton and foreign inclusions), body density, porosity, and mesohyl TEM for the high microbial abundance/low microbial abundance status. Additionally, we estimated the sponge pumping rate by measuring the excurrent velocity, the abundance of individual pumping units and cells, i.e., choanocyte chambers and choanocytes, and also carried out a morphometric analysis of aquiferous structures. The excurrent velocity and the oscular flow rates showed a positive relationship with the oscular crosssectional area for all the study species. The inorganic spicule contents by their weight as well as volume formed a major component of tissue density and higher proportions of spicules were associated with reduced aquiferous structures and lower pumping rate. The ash mass% and the ash free dry weight (AFDW %) in the sponge dry mass showed separate and distinct associations with aquiferous system variables. For example, the number of choanocytes per chamber showed a wide difference between the studied species ranging from 35.02 ± 2.44 (C. cf. cavernosa) to 120.35 ± 8.98 (I. fusca) and had a significant positive relationship with AFDW% and a negative relationship with ash mass%. This study indicates that the differences in the proportions of structural components are closely related to sponge gross morphology, anatomy, and probably body contractions, factors that influence the sponge pumping capacity.

Spatial and temporal anoxia in single-osculum Halichondria panicea demosponge explants studied with planar optodes

The water flow through sponges is regulated by their contractile behaviour including contraction and expansion of the aquiferous system, which leads to shifting oxygen levels in the sponge interior. Still, knowledge of spatial and temporal anoxia in sponges is lacking, but important in elucidating interactions between sponge hosts and their microbiomes. We combined 2-D luminescence lifetime imaging of oxygen with simultaneous time-lapse recordings of the sponge exhalant opening (osculum) to unveil temporal as well as spatial oxygen dynamics caused by contractile behaviour in single-osculum explants of the demosponge Halichondria panicea. The present study reveals an intrinsic concentric deoxygenation pattern in explants during episodes of osculum contraction generating an oxygen gradient with increasing concentrations towards the explant periphery. Four sponge explants faced 25 episodes with substantial changes in internal oxygen and anoxia which prevailed for 4.4 h of the total 92.0 h observation period. The 2-D images revealed that the total area of the explant experiencing anoxia during periods of osculum contraction–expansion varied between 0.01 and 13.22% and was on average 7.4 ± 4.4% for all sponge explants. Furthermore, oxygen respiration, as approximated by the rate of change of oxygen concentration during deoxygenation of the explant interior, was similar throughout the oxic parts of the explant base. The resolved 2-D dynamics provide an unprecedented insight into the internal O2 distribution of sponges and complement the traditional point measurements of oxygen sensors.

The Hexactinellid Deep-Water Sponge Vazella pourtalesii (Schmidt, 1870) (Rossellidae) Copes With Temporarily Elevated Concentrations of Suspended Natural Sediment

Plumes of re-suspended sediment potentially smother and clog the aquiferous system of filter-feeding sponges with unknown implications for their health. For the first time, we examined the physiological responses of repeated exposure to natural sediment in the glass sponge Vazella pourtalesii, which forms dense sponge grounds in Emerald Basin off Nova Scotia, Canada. Ex situ chamber-based measurements of bacterial clearance and oxygen consumption (respiration) rates indicated that individuals subjected to elevated concentrations of suspended sediment expressed normal clearance and respiration rates over 7 days of sediment exposure, indicating an ability to cope with elevated concentrations of indigestible sediment particles. However, clearance rates significantly declined after 14 days of sediment exposure, suggesting an inability to cope with long-term exposure to increased sediment load. Therefore, long-term exposure to elevated concentrations of suspended sediment should be avoided in order to minimize adverse effects on the abundant Vazella sponge grounds.

Hydrodynamics of sponge pumps and evolution of the sponge body plan

Sponges are suspension feeders that filter vast amounts of water. Pumping is carried out by flagellated chambers that are connected to an inhalant and exhalant canal system. In ‘leucon’ sponges with relatively high-pressure resistance due to a complex and narrow canal system, pumping and filtering are only possible owing to the presence of a gasket-like structure (forming a canopy above the collar filters). Here, we combine numerical and experimental work and demonstrate how sponges that lack such sealing elements are able to efficiently pump and force the flagella-driven flow through their collar filter, thanks to the formation of a ‘hydrodynamic gasket’ above the collar. Our findings link the architecture of flagellated chambers to that of the canal system, and lend support to the current view that the sponge aquiferous system evolved from an open-type filtration system, and that the first metazoans were filter feeders.

Dining on DOM: Stimulus for the Origin of Metazoan Life?

The most widely accepted scientific theory for the origin of life on Earth is that prokaryotic microbes evolved from simple organic compounds in seawater under anoxic conditions. For about 1 billion years thereafter, these microbes consumed the same dissolved organic matter (DOM) from which they had evolved before scarcity of DOM forced the evolution of cyanobacterial photosynthesis followed by eukaryosis. Could the more efficient consumption of DOM have also stimulated the subsequent origin of multicellular animal life? In this report, we synthesize past and recent evidence to propose the “DOM uptake hypothesis” for the origin of metazoans. A choanoflagellate-like protozoan was the likely ancestor of the first sponge-like metazoan to evolve on Earth. Choanoflagellates have outwardly facing flagellae that are subject to viscous water movement, while sponges have choanocytes in chambers with flagellae directed to pump water with greater fluidity across an aquiferous system with a huge cellular surface area. While generally considered particle feeders, both choanoflagellates and sponges absorb DOM, with some sponges relying on DOM for as much as 90% of their diet. We propose that the earliest metazoans may have evolved to survive the dire nutritional conditions of the Cryogenian “snow-ball Earth” period (~700 million years ago) by developing a body plan with the enhanced ability to absorb low concentrations of DOM in seawater from sources such as the viral lysis of microbes, exudates of benthic stromatolites, or refractory DOM compounds. Additionally, species of extant sponges that have a high abundance of microbes living in their bodies consume the greatest amounts of DOM, suggesting that the DOM uptake hypothesis may also be dependent on microbial symbiosis.

Invasive green algae in a western Mediterranean Marine Protected Area: interaction of photophilous sponges with Caulerpa cylindracea

We report on the relationships between some conspicuous Mediterranean photophilous sponge species and Caulerpa cylindracea, a non-indigenous species. A diversification of defence strategies and behaviour is highlighted in target species belonging to different orders of Demospongiae from a western Mediterranean Marine Protected Area (NW Sardinian Sea). Caulerpa cylindracea displays a strongly invasive behaviour during body colonization of the Irciniidae Sarcotragus spinosulus and Ircinia retidermata (order Dictyoceratida). These sponges possess pre-adaptive defensive morpho-functional and physiological traits enabling them to partly withstand algal invasion. Also Aplysina aerophoba (order Verongiida) seems to be able to control colonization. Successful anti-Caulerpa strategies characterize the rarely affected Crambe crambe (order Poecilosclerida). Species-specific competitive strategies are displayed at different levels of body architecture, behaviour and physiology by native sponge species. The invasion patterns on sponges, the invasion dynamics in 2016–2017 and topographic distribution of C. cylindracea on S. spinosulus confirm this algal species as a threat, with potential long-term effects on sponge assemblages. Data suggest other kinds of poorly investigated synergic stressors affecting these habitat-forming species. Defence strategies of sponge species take the form of: (1) passive deterrence by morpho-functional pre-adaptive traits as growth form, biomass amount, surface traits, and microhabitat within the sponges' aquiferous system; (2) active physiological defence, whereby the morphology/anatomy of the sponge body is adapted to control invaders, by body remodelling and regenerative processes within the aquiferous system and at the sponge surface; (3) presumed active chemical defence by exudation processes of bioactive compounds.

A new species of Baikal endemic sponges (Porifera, Demospongiae, Spongillida, Lubomirskiidae)

This paper reports on a new species of the Baikal endemic sponge (fam. Lubomirskiidae) Swartschewskia khanaevisp. nov. The description of this species is based on morphological and molecular data (ITS and mitochondrial IGRs). Morphologically, S. khanaevisp. nov. differs from S. papyracea by loose tracts arranged in an irregular network as well as the presence on strongyles of compound spines looking like tubercles densely ornamented with simple spines. Moreover, specimens of S. khanaevisp. nov. show a peculiar structure of the aquiferous system at the body surface that may be an adaptive trait for environmental conditions. Phylogenetic analysis has revealed that S. khanaevisp. nov. forms a well-supported (0.99) monophyletic clade with S. papyracea and is allocated as its sister taxa.