Sponges as sensitive animals: sensory systems and energetics of filtration in demosponges

Abstract

Sponges (Porifera) are abundant in most marine and freshwater ecosystems, and as suspension feeders they play a crucial role in filtering the water column. Their active pumping enables them to filter up to 900 times their body volume of water per hour, recycling nutrients and coupling the benthic and pelagic communities. Despite the ecological importance of sponge filter feeding, little is known about how sponges control the water flow through their canal system or how much energy it costs to filter the water. Sponges lack conventional muscles and nervous tissue, yet respond to stimuli through coordinated behaviours. Here, I show the presence of non-motile cilia in the canal system of sponges and study their role as flow sensors. I demonstrate that molecules known to block cationic channels in sensory cilia in other organisms reduce or eliminate sponge behaviour. In addition, removal of the cilia using chloral hydrate eliminates sponge contractions, suggesting the cilia are flow sensors and involved in controlling water flow through the canal system. Sponges have long been considered textbook examples of animals that use current-induced flow. I show evidence that suggests some species of demosponge do not use current-induced flow; rather, they respond behaviourally to increased ambient currents by reducing their pumping volume. Using a morphometric model of the canal system, I also show that filter feeding may be more energetically costly than previously thought. Measurements of pumping volume and oxygen drawdown in five species of demosponges show that pumping rates are variable within and between species, with more oxygen consumed the greater the pumping volume. Together, these data suggest that sponges have a lot of control over the volume of water pumped, which may be an adaptation to reduce the energetic cost of filtration in times of high stress.