Adhesive contact and protein elastic modulus tune orb weaving spider glue droplet biomechanics to habitat humidity

Tiny glue droplets along the viscous capture threads of spider orb webs prevent insects from escaping. Each droplet is formed of a protein core surrounded by a hygroscopic aqueous layer, which cause the droplet's adhesion to change with humidity. As an insect struggles to escape the web, a thread's viscoelastic core proteins extend, transferring adhesive forces to the thread's support fibers. Maximum adhesive force is achieved when absorbed atmospheric moisture allows a flattened droplet to establish sufficient adhesive contact while maintaining the core protein cohesion necessary for force transfer. We examined the relationship between these droplet properties and adhesive force and the work of extending droplets at five relative humidities in twelve species that occupy habitats which have different humidities. A regression analysis that included both flattened droplet area and core protein elastic modulus described droplet adhesion, but the model was degraded when core protein area was substituted for droplet. Species from low humidity habitats expressed greater adhesion at lower humidities, whereas species from high humidity habitats expressed greater adhesion at high humidities. Our results suggest a general model of droplet adhesion with two adhesion peaks, one for low humidity species, which occurs when increasing droplet area and decreasing protein cohesion intersect, and another for high humidity species, which occurs when area and cohesion have diverged maximally. These dual peaks in adhesive force explain why some species from intermediate and high humidity habitats express high adhesion at several humidities. STATEMENT OF SIGNIFICANCE: We characterized the effect of humidity on the adhesion of twelve orb weaving spider species' glue droplets and showed how humidity-mediated changes in the contact area of a droplet's outer, hygroscopic aqueous layer and the stiffness of its protein core affect droplet performance. This revealed how droplet adhesion has been tuned to the humidity of a species' habitat and allowed us to revise a model that describes the environmental determinants of droplet biomechanics.