The Sponge Pump: The Role of Current Induced Flow in the Design of the Sponge Body Plan

Abstract

Sponges are suspension feeders that use flagellated collar-cells (choanocytes) to actively filter a volume of water equivalent to many times their body volume each hour. Flow through sponges is thought to be enhanced by ambient current, which induces a pressure gradient across the sponge wall, but the underlying mechanism is still unknown. Studies of sponge filtration have estimated the energetic cost of pumping to be <1% of its total metabolism implying there is little adaptive value to reducing the cost of pumping by using “passive” flow induced by the ambient current. We quantified the pumping activity and respiration of the glass sponge Aphrocallistes vastus at a 150 m deep reef in situ and in a flow flume; we also modeled the glass sponge filtration system from measurements of the aquiferous system. Excurrent flow from the sponge osculum measured in situ and in the flume were positively correlated (r>0.75) with the ambient current velocity. During short bursts of high ambient current the sponges filtered two-thirds of the total volume of water they processed daily. Our model indicates that the head loss across the sponge collar filter is 10 times higher than previously estimated. The difference is due to the resistance created by a fine protein mesh that lines the collar, which demosponges also have, but was so far overlooked. Applying our model to the in situ measurements indicates that even modest pumping rates require an energetic expenditure of at least 28% of the total in situ respiration. We suggest that due to the high cost of pumping, current-induced flow is highly beneficial but may occur only in thin walled sponges living in high flow environments. Our results call for a new look at the mechanisms underlying current-induced flow and for reevaluation of the cost of biological pumping and its evolutionary role, especially in sponges.

Trait-mediated ecosystem impacts: how morphology and size affect pumping rates of the Caribbean giant barrel sponge

“…Although it is possible for flow to be passively enhanced through the sponge by pressure gradients between the ostia and osculum generated by the Bernoulli effect and viscous entrainment (Vogel 1977(Vogel , 1994, we did not find any evidence of a relationship betweenw and ambient currents. This is consistent with the calculations of Leys et al (2011) that indicate hydraulic resistance would be too great for passive flow to occur in species such as X. muta that have thick walls and relatively long and narrow water canals . Near or total pumping cessation was also observed for approximately 21% of the sponges measured.…”

“…The energetic cost of pumping has long been thought to be low, at approximately 1% of total metabolism (Riisgård et al 1993); however, recent work suggests that metabolic costs may actually be much higher (25 to 28% of total metabolism) than previous estimates (Hadas et al 2008, Leys et al 2011. If the energetic cost of pumping by X. muta is indeed high, then changes in pumping activity may be an adaptive response to the availability of picoplanktonic prey (Leys et al 2011).…”

Elements of a ‘nervous system’ in sponges

“…Capture of prey would be best achieved by filtration and concentration of food, which favours the idea of a filter/suspension feeder arising before the evolution of complex nervous systems. If filtration was the mechanism of feeding, it may have been energetically expensive (Leys et al, 2011), so it is unlikely to have originated in deep oxygen-poor oceans. Therefore, this animal would most likely have evolved in shallow waters in competition with other flagellates and have specialized to be efficient at filtering.…”

“…The filter consists of microvilli that are linked laterally by a fine glycocalyx mesh 40-70 nm in diameter (e.g. Fjerdingstad, 1961;Leys et al, 2011;Mah et al, 2014). In sponges, and in some colonial choanoflagellates, neighbouring collars are also joined near the upper end by a second mucus mesh or by cells (Weissenfels, 1992).…”

“…Glass sponges can contract but very slowly (Nickel, 2010), and contraction may not be effective to prevent damage by a sudden resuspension event. Our recent work (Leys et al, 2011) suggests that the high cost of pumping may have led, over time, to reducing the resistance through the sponge by evolving very large canals. Could the cost of filtering in the deep sea have triggered the evolution of syncytia concurrent with electrical signalling as a way to prevent intake of materials that might damage the filter?…”