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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.
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Biomechanical drivers of the evolution of butterflies and moths with a coilable proboscis
Current biomechanical models suggest that butterflies and moths use their proboscis as a drinking straw pulling nectar as a continuous liquid column. Our analyses revealed an alternative mode for fluid uptake: drinking bubble trains that help defeat drag. We combined X-ray phase-contrast imaging, optical video microscopy, micro-computed tomography, phylogenetic models of evolution and fluid mechanics models of bubble-train formation to understand the biomechanics of butterfly and moth feeding. Our models suggest that the bubble-train mechanism appeared in the early evolution of butterflies and moths with a proboscis long enough to coil. We propose that, in addition to the ability to drink a continuous column of fluid from pools, the ability to exploit fluid films by capitalizing on bubble trains would have expanded the range of available food sources, facilitating diversification of Lepidoptera.
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- Award ID(s):
- 2042937
- PAR ID:
- 10595938
- Editor(s):
- Spencer, Barrett
- Publisher / Repository:
- The Royal Society Publishing
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Edition / Version:
- 1
- Volume:
- 291
- Issue:
- 2035
- ISSN:
- 0962-8452
- Page Range / eLocation ID:
- 20240903
- Subject(s) / Keyword(s):
- evolution, Lepidoptera, proboscis, hawkmoth, feeding
- Format(s):
- Medium: X Size: 2MB Other: pdf
- Size(s):
- 2MB
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2024.0903
