Hydrophilic and Opened Canals in Honey Bee Tongue Rods Endow Elastic Structures with Multiple Functions

The honey bee (Apis mellifera L.) tongue is a sophisticated and dexterous probing device that can bend and twist, adapting to various surfaces for liquid imbibition and/or gustatory sensing. The tongue exhibits remarkable extendibility, flexibility, and durability, which may be essentially ascribed to the internal elastic rod that supports the entire tongue. However, neither the material composition nor the structural features of the rod, especially a peculiar inner canal that facilitates feeding, have been studied in relation to their function. Herein, by combining a set of imaging techniques, including optical microscopy, high-speed videography, scanning electron microscopy, micro-computed tomography (micro-CT), and confocal laser scanning microscopy, we characterize the spatial morphology, surface wettability and material composition of honey bee tongue rods. By performing mechanical testing, including atomic force microscopy, fracture testing, and finite element analysis, we provide the first evidence that the internal canal of the rod may represent a specialized structure for water retention due to the specific chemistry of resilin, which is an elastomeric protein that dominates the entire rod and renders it highly elastic, compliant and robust. Numerical simulations also suggest that the opening of the canal may facilitate larger deformations in twisting, extending the flexibility of the rod. STATEMENT OF SIGNIFICANCE: The honey bee is one of the most important pollinators around the world and is capable of foraging a wide spectrum of liquid sources by dipping into them with a miniature hairy tongue. However, there are no direct muscles distributed inside the tongue, instead, there is a conspicuous elastic rod with a hollow core. The rod extends for its full length and, according to our study, structurally reinforces the entire tongue to achieve functional versatility, and suggests a water containing function of the rod canal for maintaining the elasticity of the protein (resilin) that constitutes the rod. Our results broaden understandings of the relationship among morphology, materials science, and function of a honey bee tongue.