Towards a nanomechanical basis for temporary adhesion in barnacle cyprids ( Semibalanus balanoides )

Abstract

Cypris larvae of barnacles are able to use a rapidly reversible temporary adhesion mechanism for exploring immersed surfaces. Despite decades of research interest, the means by which cyprids maintain attachment with surfaces prior to permanent settlement remain poorly understood. Here, we present novel observations on the morphology of 'footprints' of a putative adhesive secretion deposited by cyprids during surface exploration. Atomic force microscopy (AFM) was used to image footprints at high resolution and to acquire measurements of interaction forces. R-CH 3 -and R-NH 2 -terminated glass surfaces were used for comparison of footprint morphology, and it was noted that on R-NH 2 each footprint comprised three times the volume of material deposited for footprints on R-CH 3 . Direct scaling of adhesion forces derived from AFM measurements did not adequately predict the real attachment tenacity of cyprids, and it is suggested that a mixture of 'wet' and 'dry' adhesive mechanisms may be at work in cyprid adhesion. High-resolution images of cyprid footprints are presented that correlate well with the known morphology of the attachment structures.

Atomic force microscopy of the morphology and mechanical behaviour of barnacle cyprid footprint proteins at the nanoscale

“…The total surface coverage of an average footprint was 4.1 + 0.6 Â 10 210 m 2 (n ¼ 19). The footprint size roughly corresponded to the diameter of the antennular disc of the cyprid (figure 1c; Phang et al 2008). The microtexture of the footprint was porous in nature with bundles of fibrils (bright features in figure 2b) and individual nanofibrils (indicated by arrows in figure 2c) observable across the contacted surface as shown in figure 2.…”

“…Using atomic force microscopy (AFM), Phang et al (2008) studied the macro-and micro-morphology of footprints deposited by Semibalanus balanoides. The footprint deposits of S. balanoides were composed of bundles of proteinaceous nanofibrils with heights varying between 7 and 150 nm.…”

Novel application of imaging surface plasmon resonance for in situ studies of the surface exploration of marine organisms

“…4 Neither of these techniques, however, allow for real time observation of the exploratory behavior of the organisms in situ. SEM and SPM are also less suitable for evaluation of larger surface regions.…”

“…The thickness of footprints from S. balanoides has been previously estimated, by atomic force microscopy, to fall between 5 and 19 nm, depending on the surface. 4 In future applications of this technique, we will evaluate the behavior and adhesive interactions of cyprids on a diverse range of substrates with controlled chemistry before continuing with other test species. In time, it is expected that this approach will yield important information regarding the adhesion of such organisms to specific substrates and, thus, inform the development of surfaces to which settlement is impossible.…”

Barnacle biology before, during and after settlement and metamorphosis: a study of the interface

“…Mechanisms of barnacle attachment via fluids that undergo curing have garnered scientific interest for applications to control biofouling in industrial (Callow and Callow, 2002;Holm, 2012) and medical contexts (Shivapooja et al, 2013) and bioinspired glues that cure in aqueous environments (Joseph et al, 2011;Kamino, 2013). First, the barnacle cyprid attaches to the substratum via a permanent adhesive, released from cement glands through the two walking appendages, a pair of antennules, embedding them completely, creating an adhesive plaque that anchors them in place (Knight-Jones and Crisp, 1953;Crisp, 1960;Walker, 1971Walker, , 1973Yule and Walker, 1985;Mullineaux and Butman, 1991;Matsumura et al, 1998;Phang et al, 2008;Gohad et al, 2012Gohad et al, , 2014Aldred et al, 2013). The subsequent phases of settlement and metamorphosis for acorn (balanomorph) barnacles involve major changes to the body plan and shape, resulting in a disk-shaped basis parallel to the substratum as a juvenile.…”