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Physical Determinants of Fluid-Feeding in Insects

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Fluid feeders represent more than half of the world’s insect species. We review current understanding of the physics of fluid-feeding, from the perspective of wetting, capillarity, and fluid mechanics. We feature butterflies and moths (Lepidoptera) as representative fluid-feeding insects. Fluid uptake by live butterflies is experimentally explained based on X-ray imaging and high-speed optical microscopy and is augmented by modeling and by mechanical and physicochemical characterization of biomaterials. Wetting properties of the lepidopteran proboscis are reviewed, and a classification of proboscis morphology and wetting characteristics is proposed. The porous and fibrous structure of the mouthparts is important in determining the dietary habits of fluid-feeding insects. The fluid mechanics of liquid uptake by insects cannot be explained by a simple Hagen–Poiseuille flow scenario of a drinking-straw model. Fluid-feeding insects expend muscular energy in moving fluid through the proboscis or through the sucking pump, depending primarily on the ratio of the proboscis length to the food canal diameter. A general four-step model of fluid-feeding is proposed, which involves wetting, dewetting, absorbing, and pumping. The physics of fluid-feeding is important for understanding the evolution of sucking mouthparts and, consequently, insect diversification through development of new fluid-feeding habits.
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... This can be achieved in various ways, like the triradiate sucking pharynx of tardigrades and velvet worms (4), by peristaltic contraction of the gut as in Pauropoda (5), or by one or several more complex pumping chambers as in arachnids (6), parasitic crustaceans (7), and many insects (8). Complex pumping organs for fluid feeding are most diverse and best studied in fluidfeeding insects, in which they evolved independently in several major lineages contributing to half the insect diversity (9,10). In most fluid-feeding insects, a proboscis, formed by the mouthparts, is combined with a pumping chamber, which has a similar architecture in several orders (11), and might have played a role in the diversification of insects (12). ...
... During fluid intake, the posterior sphincter muscle closes the sucking pump posteriorly in Polyzoniida, Siphonocryptida, and Siphonorhinidae, similar to Lepidoptera (35,43). When the sphincter muscle relaxes, the content of the sucking pump is emptied into the foregut passively by the elastic retraction of the dorsal wall in Siphonophorida, as is the case in Hemiptera and Diptera (34,44,45), or actively by the action of muscles dorsally of the chamber, which are only present in Polyzoniida and Siphonocryptida and might function similarly to the compressor muscles spanning across the roof of the pumping chamber in Lepidoptera (10,35) and in some Hymenoptera (37,46,47) and Coleoptera (42,48,49). A mechanism closing the sucking pump anteriorly to prevent fluid flow out of the mouthparts was reported for butterflies, moths, and Hemiptera (43, 44) but could not be identified in the studied millipedes. ...
... Fluid intake might be further facilitated by capillary forces acting at the minute slit-like opening of the preoral chamber. The minute opening of the preoral chamber, with an incised labrum, results in capillary forces, which are sufficient to fill even the elongated beak of Siphonophoridae, as is the case in butterflies (10). The upper estimate of the height of water that rises within the proboscis of Siphonophorida is more than 4 m for a beak with a diameter of 7 m, which surpasses the beak length by multiples and suggests that no suction pressure is needed to fill the proboscis. ...
Article
We report fluid feeding with a sucking pump in the arthropod class Diplopoda, using a combination of synchrotron tomography, histology, electron microscopy, and three-dimensional reconstructions. Within the head of nine species of the enigmatic Colobognatha, we found a pumping chamber, which acts as positive displacement pump and is notably similar to that of insects, showing even fine structural convergences. The sucking pump of these millipedes works together with protractible mouthparts and externally secreted saliva for the acquisition of liquid food. Fluid feeding is one of the great evolutionary innovations of terrestrial arthropods, and our study suggests that it evolved with similar biomechanical solutions convergent across all major arthropod taxa. While fluid-feeding insects are megadiverse today, it remains unclear why other lineages, such as Colobognatha, are comparably species poor.
... Fluid uptake with the proboscis is mainly comprised of four steps: wetting, dewetting, absorbing, and pumping [50,51]. Many physical determinants represent the fundamental architecture of the proboscis affecting fluid uptake [52]. For example, the absorption efficiency is affected by increased resistance from tapering of the food canal in the drinking region and the viscous resistance of the membranes spreading along the food canal [46,49]. ...
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... The problem concerns not only engineers. Mouth parts of many insects are fiber-like and the process of insect feeding somewhat resembles a process of fiber dip coating [59]. Therefore, the results of this work can be used for analysis of insect behavior during feeding. ...
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