The moth specialist spider Cyrtarachne akirai uses prey scales to increase adhesion.

Contaminants decrease adhesive strength by interfering with substrate contact. Spider webs adhering to moths present an ideal model to investigate how natural adhesives overcome contamination because moths' sacrificial layer of scales rubs off on sticky silk, facilitating escape. However, Cyrtarachninae spiders have evolved gluey capture threads that adhere well to moths. Cyrtarachne capture threads contain large glue droplets oversaturated with water, readily flowing but also prone to drying out. Here, we compare the spreading and adhesion of Cyrtarachne akirai glue on intact mothwings, denuded cuticle and glass to the glue of a common orb-weaving spider, Larinioides cornutus, to understand how C. akirai glue overcomes dirty surfaces. Videos show that C. akirai's glue spreading accelerates along the underlying moth cuticle after the glue seeps beneath the moth scales-not seen on denuded cuticle or hydrophilic glass. Larinioides cornutus glue droplets failed to penetrate the moth scales, their force of adhesion thus limited by the strength of attachment of scales to the cuticle. The large size and low viscosity of C. akirai glue droplets function together to use the three-dimensional topography of the moth's scales against itself via capillary forces. Infrared spectroscopy shows C. akirai glue droplets readily lose free-flowing water. We hypothesize that this loss of water leads to increased viscosity during spreading, increasing cohesive forces during pull-off. This glue's two-phase behaviour shows how natural selection can leverage a defensive specialization of prey against themselves and highlights a new design principle for synthetic adhesives for adhering to troublesome surfaces.