![A) Moth Symmerista albifrons (Notodontidae), with (B) the proboscis; scale bar = 150 m. C) half of the proboscis; scale bar = 50 m. This surface microsculpture typifies a limiting case of smooth bumps interspersed with narrow valleys. D) Carolina sphinx moth (Manduca sexta). E) Part of its ~ 7-cm long proboscis showing smoothed bumps interspersed with wide valleys. (A by Andy Reago and Chrissy McClarren [CC BY 2.0 (https://creativecommons.org/licenses/by/2.0)], via Wikimedia Commons; B, C, from Kornev et al., 2017 [CC BY 4.0 (https://creativecommons.org/licenses/by/4.0)]; D courtesy of C. Zhang; E by authors).](https://www.researchgate.net/profile/Konstantin-Kornev-2/publication/337854621/figure/fig4/AS:836878114779139@1576538699763/A-Moth-Symmerista-albifrons-Notodontidae-with-B-the-proboscis-scale-bar-150-m_Q320.jpg)
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Physical Determinants of Fluid-Feeding in Insects
Abstract and Figures
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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... Drinking straw models of fluid uptake assume that hawkmoths drink nectar, that is, nectar continuously flows through the proboscis to the sucking pump [5,6]. Thus, to defeat the viscous drag of nectar passing through the proboscis, hawkmoths should create a large pressure differential, requiring large sucking pumps with stronger, more voluminous muscles as proboscis size increases (figure 1; [5,6]). ...
... Drinking straw models of fluid uptake assume that hawkmoths drink nectar, that is, nectar continuously flows through the proboscis to the sucking pump [5,6]. Thus, to defeat the viscous drag of nectar passing through the proboscis, hawkmoths should create a large pressure differential, requiring large sucking pumps with stronger, more voluminous muscles as proboscis size increases (figure 1; [5,6]). In the alternative model to explain rapid drinking [4], fluid enters the food canal through legular bands so that neither size of the sucking pump nor muscle volume would limit feeding rate. ...
... Anatomical features related to biomechanics of the sucking pump-proboscis complex of adult Lepidoptera have been discussed [5,6,9]. We focus on the most critical structures (figure 1e) in operation of the sucking pump. ...
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.
... 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. ...
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.
... More than half of all known insects on Earth-over 500,000 species-are fluid feeders (1). Among them, nectar feeders have attracted the attention of scientists since Darwin predicted, well before its discovery, the existence of a specific orchid corresponding to the extraordinarily long proboscis of sphinx moth (2,3). How nectar-feeding insects use their elaborate mouthparts to interact with the great variety of flower structures remains an important question in evolutionary biology, ecology, and biomechanics (4-7). ...
... , we obtain the expression of ΔP in terms of Ẇ . Substituting this last relation into Eqs. 1 and 2, we obtain [3] Therefore, the liquid intake rate decreased when the liquid meniscus level x is larger than: ...
The feeding mechanisms of animals constrain the spectrum of resources that they can exploit profitably. For floral nectar eaters, both corolla depth and nectar properties have marked influence on foraging choices. We report the multiple strategies used by honey bees to efficiently extract nectar at the range of sugar concentrations and corolla depths they face in nature. Honey bees can collect nectar by dipping their hairy tongues or capillary loading when lapping it, or they can attach the tongue to the wall of long corollas and directly suck the nectar along the tongue sides. The honey bee feeding apparatus is unveiled as a multifunctional tool that can switch between lapping and sucking nectar according to the instantaneous ingesting efficiency, which is determined by the interplay of nectar-mouth distance and sugar concentration. These versatile feeding mechanisms allow honey bees to extract nectar efficiently from a wider range of floral resources than previously appreciated and endow them with remarkable adaptability to diverse foraging environments.
... The obtained diagrams and experimental protocols could be used in many engineering applications dealing with filtration [1,5] and printing [35,36] as well in many biological applications [15,[37][38][39][40]. For example, hovering hawkmoths with long proboscises benefit from pulling out a nectar film on its surface [40]. ...
... The obtained diagrams and experimental protocols could be used in many engineering applications dealing with filtration [1,5] and printing [35,36] as well in many biological applications [15,[37][38][39][40]. For example, hovering hawkmoths with long proboscises benefit from pulling out a nectar film on its surface [40]. When the insect withdraws its proboscis from the flower, this film could be sipped up during flight. ...
... Such morphological fine-tuning occurs in skipper butterflies where interconnected organs of the feeding apparatus inside the head and the proboscis have been found (Krenn & Bauder, 2017). It has been suggested that the pressure drop produced by the suction pump correlates positively with the flow rate of the liquid passing through the food canal (Kornev & Adler, 2019). In this context, the remarkably large food canal in A. atropos could additionally help to overcome the flow resistance of the highly viscose honey (Garcia et al., 2005). ...
... This is in line with the biophysical considerations of Kornev and Adler (2019) that insects with very short proboscises expend more energy for swallowing than for the up-take of liquids through the food canal. ...
The morphology of the proboscis and associated feeding organs was studied in several nectar‐feeding hawk moths, as well as a specialized honey‐feeder and two supposedly non‐feeding species. The proboscis lengths ranged from a few millimeters to more than 200 mm. Despite the variation in proboscis length and feeding strategy, the principle external and internal composition of the galeae, the stipes pump and the suction pump were similar across all species. The morphology of the smooth and slender proboscis is highly conserved among all lineages of nectar‐feeding Sphingidae. Remarkably, they share a typical arrangement of the sensilla at the tip. The number and length of sensilla styloconica are independent from proboscis length. A unique proboscis morphology was found in the honey‐feeding species Acherontia atropos. Here, the distinctly pointed apex displays a large subterminal opening of the food canal, and thus characterizes a novel type of piercing proboscis in Lepidoptera. In the probably non‐feeding species, the rudimentary galeae are not interlocked and the apex lacks sensilla styloconica; galeal muscles however, are present. All studied species demonstrate an identical anatomy of the stipes‐ and suction pump, regardless of proboscis length and diet. Even supposedly non‐feeding Sphingidae possess all organs of the feeding apparatus, suggesting that their proboscis rudiments might still be functional. The morphometric analyses indicate significant positive correlations between galea lumen volume and stipes muscle volume as well as the volume of the food canal and the muscular volume of the suction pump. Size correlations of these functionally connected organs reflect morphological fine‐tuning in the evolution of proboscis length and function. This article is protected by copyright. All rights reserved.
... The time interval between these runs was set at 10 min, so the water film on the proboscis had time to evaporate and the advancing contact angle could be measured. The validity of this protocol was previously confirmed using painted lady butterflies (Vanessa cardui L.; Kornev and Adler, 2019;Lehnert et al., 2013). All videos were recorded at an average of 13.45 frames s −1 to show the changing meniscus profile on the left and right sides of the proboscis at different positions. ...
Hovering hawkmoths expend significant energy while feeding, which should select for greater feeding efficiency. Although increased feeding efficiency has been implicitly assumed, it has never been assessed. We hypothesized that hawkmoths have proboscises specialized for gathering nectar passively. Using contact angle and capillary pressure to evaluate capillary action of the proboscis, we conducted a comparative analysis of wetting and absorption properties for 13 species of hawkmoths. We showed that all 13 species have a hydrophilic proboscis. In contradistinction, the proboscises of all other tested lepidopteran species have a wetting dichotomy with only the distal ∼10% hydrophilic. Longer proboscises are more wettable, suggesting that species of hawkmoths with long proboscises are more efficient at acquiring nectar by the proboscis surface than are species with shorter proboscises. All hawkmoth species also show strong capillary pressures which, together with the feeding behaviors we observed, ensure that nectar will be delivered to the food canal efficiently. The patterns we found suggest that different subfamilies of hawkmoths use different feeding strategies. Our comparative approach reveals that hawkmoths are unique among Lepidoptera and highlights the importance of considering the physical characteristics of the proboscis to understand the evolution and diversification of hawkmoths.
... Fixing the ratio R max =R f and withdrawing the fiber from the nodoidal drop, we confirmed that an unduloidal drop could be formed, and its receding contact angle satisfies the theoretically derived condition: cos h < R f Rmax . The obtained results complete the classification of morphological configurations of axisymmetric droplets on fibers and could be used in many applications in fiber science and biology, [1][2][3][4][5][6]45,46 where one needs to evaluate the possibility of obtaining axisymmetric droplets on fibers. The developed theory significantly enriches the existing scenario of the formation of drops on fibers by introducing nodoidal FIG. 9. Experimental setup allowing to validate the models of axisymmetric droplets on fibers. ...
With the developments in nanotechnology, nanofibrous materials attract great attention as possible platforms for fluidic engineering. This requires an understanding of droplet interactions with fibers when gravity plays no significant role. This work aims to classify all possible axisymmetric configurations of droplets on fibers. The contact angle that the drop makes with the fiber surface is allowed to change from 0° to 180°. Nodoidal apple-like droplets with inverted menisci cusped toward the droplet center and unduloidal droplets with menisci cusped away from the droplet center were introduced and fully analyzed. The existing theory describing axisymmetric droplets on fibers is significantly enriched introducing new morphological configurations of droplets. It is experimentally shown that the barreled droplets could be formed on non-wettable fibers offering contact angles greater than 90°. The theory was quantitatively confirmed with hemispherical droplets formed at the end of a capillary tube and satisfying all the boundary conditions of the model. It is expected that the developed theory could be used for the design of nanofiber-based fluidic devices and for drop-on-demand technologies.
... 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]. ...
The proboscis is an important feeding organ for the glossatan moths, mainly adapted to the flower and non-flower visiting habits. The clover cutworm, Scotogramma trifolii Rottemberg, and the spotted clover moth, Protoschinia scutosa (Denis & Schiffermuller), are serious polyphagous pests, attacking numerous vegetables and crops, resulting in huge economic losses. However, the feeding behavior and mechanisms of the adult stage remain unsatisfactorily explored. In this study, the proboscis morphology of S. trifolii and P. scutosa are described in detail using scanning electron microscopy, with the aim of investigating the morphological differences and feeding behavior of these two species. The proboscises of S. trifolii and P. scutosa are similar in morphology and structure and are divided into three zones (Zone 1–3) based on the morphological changes of the dorsal legulae. Three sensillum types are located on the proboscises of both species, sensilla chaetica, sensilla basiconica, and sensilla styloconica. Significant differences were observed in the length of the proboscis and each zone between these two species, as well as in sensilla size and number. Based on the morphology of the proboscis and associated sensilla, S. trifolii and P. scutosa are potential flower visitors, which was also reinforced by the pollen observed at the proboscis tip. These results will strengthen our understanding of the structure of the proboscis related to the feeding behavior of Noctuidae.
... 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. ...
Hypothesis
The Landau-Levich-Derjaguin (LLD) theory is widely applied to predict the film thickness in the dip-coating process. However, the theory was designed only for flat plates and thin fibers. Fifty years ago, White and Tallmadge attempted to generalize the LLD theory to thick rods using a numerical solution for a static meniscus and the LLD theory to forcedly match their numeric solution with the LLD asymptotics. The White-Talmadge solution has been criticized for not being rigorous yet widely used in engineering applications mostly owing to the lack of alternative solutions. A new set of experiments significantly expanding the range of White-Tallmadge conditions showed that their theory cannot explain the experimental results. We then hypothesized that the results of LLD theory can be improved by restoring the non-linear meniscus curvature in the equation. With this modification, the obtained equation should be able to describe static menisci on any cylindrical rods and the film profiles observed at non-zero rod velocity.
Experiment
To test the hypothesis, we distinguished capillary forces from viscous forces by running experiments with different rods and at different withdrawal velocities and video tracking the menisci profiles and measuring the weight of deposited films. The values of film thickness were then fitted with a mathematical model based on the modified LLD equation. We also fitted the meniscus profiles.
Findings
The results show that the derived equation allows one to reproduce the results of the LLD theory and go far beyond those to include rods of different radii. A new set of experimental data together with the White-Tallmadge experimental data are explained with the modified LLD theory. A set of simple formulas approximating numeric results have been derived. These formulas can be used in engineering applications for the prediction of the coating thickness.
Proboscises of many fluid-feeding insects share a common architecture: they have a partially open food canal along their length. This feature has never been discussed in relation to the feeding mechanism. We formulated and solved a fluid mechanics model of fluid uptake and estimated the time required to completely fill the food canal of the entire proboscis through the openings along its length. Butterflies and moths are taken as illustrative and representative of fluid-feeding insects. We demonstrated that the proposed mechanism of filling the proboscis with fluid through permeable lengthwise bands, in association with a thin film of saliva in the food canal, offers a competitive pathway for fluid uptake. Compared with the conventional mechanism of fluid uptake through apically restricted openings, the new mechanism provides a faster rate of fluid uptake, especially for long-tongued insects. Accordingly, long-tongued insects with permeable lengthwise bands would be able to more rapidly exploit a broader range of liquids in the form of films, pools, and discontinuous columns, thereby conserving energy and minimizing exposure to predators, particularly for hovering insects.
The proboscis of butterflies and moths consists of two C-shaped fibres, the galeae, which are united after the insect emerges from the pupa. We observed that proboscis self-assembly is facilitated by discharge of saliva. In contrast with vertebrate saliva, butterfly saliva is not slimy and is an almost inviscid, water-like fluid. Butterfly saliva, therefore, cannot offer any viscoelastic adhesiveness. We hypothesized that capillary forces are responsible for helping butterflies and moths pull and hold their galeae together while uniting them mechanically. Theoretical analysis supported by X-ray micro-computed tomography on columnar liquid bridges suggests that both concave and convex liquid bridges are able to pull the galeae together. Theoretical and experimental analyses of capillary forces acting on natural and artificial proboscises show that these forces are sufficiently high to hold the galeae together.
Insect wings consist almost entirely of lifeless cuticle; yet their veins host a complex multimodal sensory apparatus and other tissues that require a continuous supply of water, nutrients and oxygen. This review provides a survey of the various living components in insect wings, as well as the specific contribution of the circulatory and tracheal systems to provide all essential substances. In most insects, hemolymph circulates through the veinal network in a loop flow caused by the contraction of accessory pulsatile organs in the thorax. In other insects, hemolymph oscillates into and out of the wings due to the complex interaction of several factors, such as heartbeat reversal, intermittent pumping of the accessory pulsatile organs in the thorax, and the elasticity of the wall of a special type of tracheae. A practically unexplored subject is the need for continuous hydration of the wing cuticle to retain its flexibility and toughness, including the associated problem of water loss due to evaporation. Also, widely neglected is the influence of the hemolymph mass and the circulating flow in the veins on the aerodynamic properties of insect wings during flight. Ventilation of the extraordinarily long wing tracheae is probably accomplished by intricate interactions with the circulatory system, and by the exchange of oxygen via cutaneous respiration.
Mosquitoes transport liquid foods into the body using two muscular pumps in the head. In normal drinking, these pumps reciprocate in a stereotyped pattern of oscillation, with a high frequency but small stroke volume. Do mosquitoes modulate their neuromotor programs for pumping to produce different drinking modes? More broadly, what are the mechanical consequences of a two-pump system in insects? To address these questions, we used synchrotron x-ray imaging and fluid mechanical modeling to investigate drinking performance in mosquitoes. X-ray imaging of the pumps during drinking revealed two modes of pumping: continuous reciprocation with multiple small strokes,
and a newly discovered ‘burst mode’ involving a single, large-volume stroke. Results from modeling
demonstrate that burst mode pumping creates a very large pressure drop and high volume flow rate,
but requires a massive increase in power, suggesting that continuous pumping is more economical for drinking. Modeling also demonstrates that, from one mode of pumping to the other, the mechanical role of the individual pumps changes. These results suggest that the advantage of a two-pump system in insects lies in its flexibility, enabling the animal to pump efficiently or powerfully as demanded by environmental considerations.
Proboscises of butterflies are modelled as elliptical hollow fibres that can be bent into coils. The behaviour of coating films on such complex fibres is investigated to explain the remarkable ability of these insects to control liquid collection after dipping the proboscis into a flower or pressing and mopping it over a food source. By using a thin-film approximation with the air-liquid interface positioned almost parallel to the fibre surface, capillary pressure was estimated from the profile of the fibre surfaces supporting the films. The film is always unstable and the proboscis shape and movements have adaptive value in collecting fluid: coiling and bending of proboscises of butterflies and moths facilitate fluid collection. Some practical applications of this effect are discussed with regard to fibre engineering.
On the basis of an assemblage of fossilized wing scales recovered from latest Triassic and earliest Jurassic sediments from northern Germany, we provide the earliest evidence for Lepidoptera (moths and butterflies). The diverse scales confirm a (Late) Triassic radiation of lepidopteran lineages, including the divergence of the Glossata, the clade that comprises the vast multitude of extant moths and butterflies that have a sucking proboscis. The microfossils extend the minimum calibrated age of glossatan moths by ca. 70 million years, refuting ancestral association of the group with flowering plants. Development of the proboscis may be regarded as an adaptive innovation to sucking free liquids for maintaining the insect’s water balance under arid conditions. Pollination drops secreted by a variety of Mesozoic gymnosperms may have been non-mutualistically exploited as a high-energy liquid source. The early evolution of the Lepidoptera was probably not severely interrupted by the end-Triassic biotic crisis.
