Specialized morphology and material properties make a honey bee tongue both extendible and structurally stable

The honey bee, Apis mellifera ligustica, uses the specialized tongue structured by ∼120 segmental units, coated by bushy hairs, to dip varying concentration nectar flexibly at small scales. While dipping, the segmental units elongate by 20%, coordinated with rhythmical erection of hairs, the pattern of which is demonstrated to be capable of both increasing nectar intake rate and saving energy. The compliance in the segmental units allows extension of the tongue, which however, challenges the structural stability while traveling through the viscous fluid. In this combined experimental and theoretical investigation, we apply scanning electron microscopy (SEM), confocal laser scanning microscopy (CLSM), micro-computed tomography scanning (micro-CT), atomic force microscopy (AFM), and mechanical models to reveal the structural and material specializations in a bee tongue for meeting the functionally contradictive demands. We find that each segmental unit is a complex structure, which is composed of an intersegmental membrane (ISM) and a ring-like hair base (RHB), with spatially distributed discrete changes in material properties. The combination of these two components makes the tongue multifunctional, in which the ISMs characterized by resilin-rich material make the segmental units compliant, while the RHBs with rigid sclerotized material provide stable supporting for hairs. Our study may enlighten deployable mechanisms with correlative functional components, especially the microscopic mechanisms applied in viscous fluid tranport. STATEMENT OF SIGNIFICANCE: The honey bee tongue is a versatile tool that extends to probe into varying-shaped corollas, retracting with 3,000 glossal hairs staying erected to load nectar. The combined requirement of both deformability and structural stability imposes opposing demands on structural stiffness. Here we show that glossal hairs are supported by rigid continuum ring-like hair bases, embedded in the elastic resilient intersegmental membrane, making the whole tongue both flexible and rigid at the same time. Our findings extend our understanding of relationship between morphology, material composition and biomechanics of dynamic biological surfaces, which may inspire design paradigms of multifunctional deployable mechanisms coordinating deformability and structural stability.