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Photomicrographs of butterfly proboscises (SEM). (A) Coiled proboscis of the tiger swallowtail (Papilio glaucus). (B) Cross-section of the proboscis of the monarch butterfly (Danaus plexippus) with a circular hole, the food canal, formed by the two halves (galeae). The top and bottom fence-like structures (legulae) link the two galeae together. (C) A single galea of the monarch butterfly resembles a C-shaped fiber with a semicircular C-channel, which, when united with the other half, forms a food canal (Reproduced by SPIE permission from Kornev et al., 2016).
Source publication
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...
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... proboscis of fluid-feeding insects differs structurally among species. For example, the butterfly proboscis consists of two elongated components (i.e., galeae), joined together by linking mechanisms made of fence-like structures (Fig. 2, and Chapt. 3). Fluid is transported through a food canal between the galeae (Eastham andEassa, 1955, Krenn, 2010). The proboscises of bees, house flies, and mosquitoes have different structure, often independently evolved, implying that different physical mechanisms for fluid uptake and transport might be involved (Smith, 1985, ...
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... cases, the drinking-straw model of insect proboscises fails to describe the process of fluid delivery. For example, lepidopteran proboscises do not have a sizable opening to the food canal at their apices ( Fig. 11). Lepidoptera use their legulae to hold the two galeae together and to facilitate fluid entry while restricting the entry of debris (Fig. 12D, E). The legulae are next to one another or overlap, but the legular bands are not sealed, allowing liquid to move through the interlegular slits to the food canal (Tsai et al., 2011(Tsai et al., , 2014Monaenkova et al., 2012, Lehnert et al., 20132016, Lee et al., 2014a, 2014bLee and Lee, 2014). Accordingly, Lepidoptera capitalize on ...
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... of the most common is galeal sliding (Fig. 19), also referred to as "anti-parallel movements", which may adjust the fluid-pressure differential by changing the size of the interlegular slits and terminal opening and by reducing the active, tapered length of the food canal (Kwauk, 2012, Tsai et al., 2014). Galeal sliding is also used in self-assembly of the proboscis after a lepidopteran emerges from the pupa (Krenn, 1997, Zhang et al., 2018a). Moths that pierce animal and plant tissues also use this strategy (Büttiker et al., 1996). ...
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... splaying opens the distal end of the proboscis (Kwauk, 2012, Tsai et al., 2014). It could reduce the pressure differential by increasing the diameter of the tapered region. Galeal pulsing might be controlled by hemolymph pressure, similar to processes involved in coiling and uncoiling the proboscis. In Fig. 20, we reproduce the flow maps around proboscises of butterflies and mosquitoes drinking from a pool of water ( Lee et al., 2014b). Water enters the food canal from the interlegular slits at the proximal part of the drinking region. The authors did not study the cause of the flow in this part of the drinking region; however, the opening ...
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... et al., 2012). Galeal sliding is typically slower (0.1-90.0 sec) and, therefore, can be independent of the pump; thus, the proboscis could remain open for multiple pump cycles. Galeal pulsing occurs faster than the contraction-expansion rate of the sucking pump, possibly facilitating flow during the first half of the cycle when the pump is open. Fig. 20 supports this hypothesis, but more experiments are required to test ...
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... than the radius of the food canal, í µí°¿ í µí±í µí± >> Rp, to neglect the effect of fluid flow at the end menisci. If the insect drinks continuous liquid columns, a pressure drop, í µí±, results, which is distributed linearly over the entire length of the proboscis, í µí°¿ í µí± , creating a constant pressure gradient, í µí±/í µí°¿ í µí± (Fig. 21). If the insect drinks a bubble train of í µí± liquid bridges, each of í µí°¿ í µí±í µí± length, separated by N+1 bubbles, each of í µí°¿ í µí± length, the pressure drops only over the liquid bridge with the gradient í µí± í µí±í µí±¡ /í µí°¿ í µí± , where í µí± í µí±í µí±¡ = í µí± í µí± − í µí± í µí±+1 . Assuming that ...
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... rate is maximum, (B) when the butterfly pushes water out at a maximum rate, and (C) when the butterfly is at rest and neither takes water in nor out. (D-F) Phase-averaged velocity fields around the proboscis of a mosquito, corresponding to intake, discharge, and resting, respectively. (Reproduced from Lee et al., 2014b by permission of Elsevier). Fig. 21. Schematic of the pressure distribution in a proboscis with a bubble train and with a continuous liquid column, assuming that the mean velocity of the liquid bridges is the same as that of the column. In each bubble, the pressure is constant, and the n-th bubble has pressure Pn. The liquid bridge has length í µí°¿ í µí±í µí± and the ...
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... pump mechanics were first explained by Bennet-Clark (1963), who proposed an informative model of the buccal chamber of Rhodnius prolixus as a U-shaped dish covered by a piston (plunger) moving up and down through the central opening of the dish (Fig. 22). This model was generalized to other fluidfeeding insects, with the U-shaped cross-section of the pump as the main geometrical motif ( Daniel et al., 1989, Lehane, 2005, Vogel, 2007, Bach et al., 2015, but with cylindrical and rectangular buccal chambers treated separately (Fig. 22). The plunger is assumed to fit the U-shaped floor ...
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... moving up and down through the central opening of the dish (Fig. 22). This model was generalized to other fluidfeeding insects, with the U-shaped cross-section of the pump as the main geometrical motif ( Daniel et al., 1989, Lehane, 2005, Vogel, 2007, Bach et al., 2015, but with cylindrical and rectangular buccal chambers treated separately (Fig. 22). The plunger is assumed to fit the U-shaped floor tightly so that the pump height, ℎ, in the z-direction perpendicular to the floor remains smaller than other scales (Table 1). Bennet-Clark (1963) and others did not discuss the mechanism of suction pressure generation, assuming that the pressure in the pump is uniform and its magnitude ...
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... separates the plunger from the chamber bottom, and the plunger is set to move, due to the cohesion of the liquid particles, the whole liquid layer is engaged in the flow. A theoretical analysis of flow in the buccal chamber reveals that movement of the plunger establishes a non-homogeneous pressure distribution in the pump ( Kornev et al., 2017) (Fig. 23A, B). When the plunger is moving up and opening the chamber, and the distance between the plunger and chamber floor remains small, ℎ/í µí± → 0, it generates a suction (negative with respect to the atmospheric) pressure written as Ratio AB/R is equal to 2θ. The model pump has opening AB connecting the chamber with the proboscis and opening ...
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... í µí°´=µí°´= í µí°µ = í µí± 2 , í µí± = í µí±¥/í µí± , í µí± = í µí±¦/í µí± , í µí± is the chamber radius, and for a rectangular chamber í µí°´=µí°´= í µí°¿ 2 and í µí°µ = í µí±/(í µí¼í µí°¿), í µí± = í µí±¥/í µí°¿, í µí± = í µí±¦/í µí°¿, and í µí°¿, í µí± are the chamber length and width, respectively. Other parameters are defined in Fig. 22. The dimensionless function í µí± is plotted in Fig. 23A for a cylindrical chamber; more details on the behavior of pressure in cylindrical and rectangular chambers are given by Kornev et al. (2017). The function í µí± does not depend on any physical parameters of the fluid, but depends only on the ratio of the food canal diameter í ...
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... , í µí± = í µí±¦/í µí± , í µí± is the chamber radius, and for a rectangular chamber í µí°´=µí°´= í µí°¿ 2 and í µí°µ = í µí±/(í µí¼í µí°¿), í µí± = í µí±¥/í µí°¿, í µí± = í µí±¦/í µí°¿, and í µí°¿, í µí± are the chamber length and width, respectively. Other parameters are defined in Fig. 22. The dimensionless function í µí± is plotted in Fig. 23A for a cylindrical chamber; more details on the behavior of pressure in cylindrical and rectangular chambers are given by Kornev et al. (2017). The function í µí± does not depend on any physical parameters of the fluid, but depends only on the ratio of the food canal diameter í µí± í µí± = |í µí°´í µí°µ| to the cylinder radius í µí± ...
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... parameters of the fluid, but depends only on the ratio of the food canal diameter í µí± í µí± = |í µí°´í µí°µ| to the cylinder radius í µí± ; for a rectangular chamber, this function depends on the chamber width to length ratio í µí±/í µí°¿ and food canal diameter í µí± í µí± = |í µí°´í µí°µ| to the chamber length ratio |í µí°´í µí°µ|/í µí°¿ (Fig. ...
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... depends only on the in-plane coordinates í µí±¥ and í µí±¦. This factorization suggests that the in-plane pressure pattern remains universal; the rate of plunger movement and the instantaneous height of the plunger affect the magnitude of the generated pressure, but they do not change the shape and positions of the lines of equal pressure in Fig. 23. As follows from Darcy's law, the spatial pattern of the in-plane fluid velocity, which depends on the pressure gradient, remains the same during the suction stroke; only the magnitude of velocity ...
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... can be classified according to their mechanism of energy dissipation by introducing two dimensionless parameters, í µí± = í µí°¿ í µí± ℎ 3 /í µí± í µí± 4 and g = dp /L. Fig. 23C specifies the insects that dissipate their muscular energy mostly in transporting fluids through their sucking pump versus their proboscis. The derived diagram allows the constraints of fluid mechanics on evolution of the feeding organs to be examined. Insects with a large f-factor expend most of their musculature energy fighting ...
Citations
... 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.
... 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.
... 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.
... 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.
... 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.
... 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.
