Key features enabling water repellency in velvet worm skin: Overhanging scales and carbonate-wax synergy

Nature has evolved sophisticated surface architectures to achieve non-wettability and self-cleaning performance under challenging environmental conditions. In this study, we elucidate the multiscale chemical and structural mechanisms underlying the exceptional water-repellent and anti-adhesive properties of the velvet worm Epiperipatus biolleyi. By integrating cryo-scanning electron microscopy (cryo-SEM), transmission electron microscopy (TEM), confocal Raman spectroscopy, X-ray photoelectron spectroscopy (XPS) depth profiling, X-ray diffraction (XRD), energy-dispersive X-ray spectroscopy (EDS), and contact angle measurements, we reveal a synergistic system composed of hierarchical micropapillae bearing overhanging tiptop scales and surrounded by nanowrinkles. We further show that the cuticle is biomineralized with calcium–magnesium carbonate phases beneath a waxy organic layer. This multiscale architecture yields water contact angles exceeding 130° and sustains a persistent, plastron-like gas layer upon immersion. The presence of overhanging scales with re-entrant curvature (ψ ≈ 34°), together with the surrounding nanowrinkles, inhibits wetting even under pressures higher than atmospheric pressure, as supported by COMSOL Multiphysics 2D simulations. The waxy layers that coat the micro- and nanostructures—composed primarily of long-chain fatty acid amides and fatty acids—further enhance the anti-adhesive behavior. This study also provides the first evidence in Onychophora of extensive cuticular biomineralization, where carbonate dissolution can locally liberate CO2, contributing to the formation and maintenance of a protective gas plastron around the microstructures. Together, these findings demonstrate that the integration of hierarchical micro- and nanostructures, a biomineralized cuticle, and a biochemical surface coating is essential to the unique anti-adhesive properties of E. biolleyi, underscoring its potential as a model for designing biomimetic, low-adhesion surface technologies.