The crescent cross-section and dichotomous chitin structure make the proboscis of butterflies and moths a hydraulic spring

Abstract

The proboscis of butterflies and moths is made of two C-shaped tubular strands, each with a crescent cross-section. Together, they form a food canal for fluid uptake. Each strand is sealed at the free end and blood is pumped in at the head. The accepted scenario for proboscis uncoiling assumes that intrinsic muscles deform the proboscis walls like fingers pressing a bicycle tire, decreasing the cross-sectional area and displacing blood that pushes the external walls outward, as does the air in the tire. This scenario requires the external walls of the strands to be softer than the food canal walls. We tensile-tested the proboscis of Manduca sexta hawk moths and discovered that the food canal walls are softer than the external walls, contradicting the accepted scenario. We hypothesize that the proboscis works as a hydraulic spring, requiring no muscular action to uncoil. The model supports this hypothesis: the pump pressurizes the blood, which pushes on the food canal walls, buckling them inward. The crescent edges along which the strands are connected are free to move loosening the coil and unrolling the proboscis. Using X-ray scattering and assuming the same cuticle matrix for both walls of the crescent strands, we showed that the difference in cuticular stiffnesses is achieved through a unidirectional ordering of α-chitin nanofibrils aligned mutually orthogonal in the food canal and external walls of the proboscis, making it a transversely anisotropic tubular composite and preventing buckling. This arrangement opens new engineering opportunities for multifunctional fiber-based hydraulic springs in micromachines. STATEMENT OF SIGNIFICANCE: Our discovery replaces the conventional textbook scenario of proboscis uncoiling in the manner of a tape measure triggered by muscles and blood. We emphasize the importance of the crescent-shaped cross-section, enabling the uncoiling of the proboscis by low blood pressure and recoiling by the deformed crescent bows. Small- and wide-angle synchrotron X-ray scattering revealed the dichotomous chitin nanocrystal orientation of the proboscis cuticle. Nanocrystals differentially reinforce the internal and external walls of the proboscis that experience different mechanical stresses. This hydraulic spring mechanism in proboscises can be used to engineer microfluidic devices that require coiling-uncoiling.

Keywords: Chitin; Cuticle; Lepidoptera; Proboscis; Shell mechanics; X-ray analysis.