Colloblasts act as a biomechanical sensor for suitable prey in Pleurobrachia

Abstract

Ctenophores are a group of largely-planktonic, gelatinous carnivores whose most common method of prey capture is nearly a phylum-defining trait. Tentaculate ctenophores release an unknown proteinaceous adhesive from specialised colloblast cells lining their tentacles following prey contact with the tentacles. There exist no extant studies of the mechanical properties of colloblast adhesive. We use live microscopy techniques to visualise adhesion events between Pleurobrachia pileus colloblasts and probes of different surface chemistries in response to probing with varying contact areas. We further define two mechanisms of adhesion termination upon probe retraction. Adapting a technique for measuring surface tension, we examine the adhesive strength of tentacles in the ctenophore Pleurobrachia bachei under varying pH and bonding time conditions, and demonstrate the destructive exhaustion of colloblast adhesive release. We find that colloblast-mediated adhesion is rapid, and that the bonding process is robust against shifts in ambient pH. However, we find that the Pleurobrachia colloblast adhesive system is among the weakest biological adhesive systems yet described. We place this surprising observation into a broader ecophysiological context by modeling prey capture for prey of a range of sizes. We find that limited use of colloblast adhesive with high surface area contact is suitable both for capturing appropriately sized prey and rejecting, by detachment, prey above a certain size threshold. This allows Pleurobrachia, lacking a mechanism to directly "see" potential prey they are interacting with, to invest in capturing only prey of an appropriate size, decreasing the risk of injury. Summary statementCtenophore colloblast adhesive is found to be strong, but few colloblasts are simultaneously active, producing a weakly-adhering system. A physical model demonstrates how such a system may filter unsuitable prey.