Insect Pads Research Articles

Rate-dependent adhesion together with limb collaborations facilitate grasshoppers reliable attachment under highly dynamic conditions

Dynamic attachment is indispensable for animals to cope with unexpected disturbances. Minor attention has been paid to the dynamic performance of insects' adhesive pads. Through experiments pulling whole grasshoppers off a glass rod at varying speeds, surprising findings emerged. The feet did not always maintain contact but released and then reconnected to the substrate rapidly during leg extension, potentially reducing the shock damage to pads. As the pulling speeds increased from 1 to 400mm/s, the maximum forces of single front tarsus insects and entire tarsi insects were nearly proportional to the 1/3 power of pulling speeds by 0.11 and 0.29 times, respectively. The force of some individuals could be even 800 times greater than their weight, which is unexpectedly high for smooth insect pads. This work not only helps us to understand the attachment intelligence of animals but is also informative for artificial attachment in extreme situations.

The physical properties of the stick insect pad secretion are independent of body size.

Many insects use adhesive organs to climb. The ability to cling to surfaces is advantageous but is increasingly challenged as animals grow, due to the associated reduction in surface-to-volume ratio. Previous work has demonstrated that some climbing animals overcome this scaling problem by systematically altering the maximum force per area that their adhesive pads can sustain; their adhesive organs become more efficient as they grow, an observation which is also of substantial relevance for the design of bioinspired adhesives. What is the origin of this change in efficiency? In insects, adhesive contact is mediated by a thin film of a liquid, thought to increase adhesive performance via capillary and viscous forces. Here, we use interference reflection microscopy and dewetting experiments to measure the contact angle and dewetting speed of the secretion of pre-tarsal adhesive pads of Indian stick insects, varying in mass by over two orders of magnitude. Neither contact angle nor dewetting speed change significantly with body mass, suggesting that the key physical properties of the pad secretion-its surface tension and viscosity-are size-invariant. Thus, the observed change in pad efficiency is unlikely to arise from systematic changes of the physical properties of the pad secretion; the functional role of the secretion remains unclear.

Disentangling the role of surface topography and intrinsic wettability in the prey capture mechanism of Nepenthes pitcher plants

Nepenthes pitcher plants capture prey with leaves specialised as pitfall traps. Insects are trapped when they ‘aquaplane’ on the pitcher rim (peristome), a surface structured with macroscopic and microscopic radial ridges. What is the functional significance of this hierarchical surface topography? Here, we use insect pad friction measurements, photolithography, wetting experiments and physical modelling to demonstrate that the ridges enhance the trap's efficacy by satisfying two functional demands on prey capture: Macroscopic ridges restrict lateral but enhance radial spreading of water, thereby creating continuous slippery tracks which facilitate prey capture when little water is present. Microscopic ridges, in turn, ensure that the water film between insect pad and peristome remains stable, causing insects to aquaplane. In combination, the hierarchical ridge structure hence renders the peristome wettable, and water films continuous, so avoiding the need for a strongly hydrophilic surface chemistry, which would compromise resistance to desiccation and attract detrimental contamination.

Shear-sensitive adhesion enables size-independent adhesive performance in stick insects.

The ability to climb with adhesive pads conveys significant advantages and is widespread in the animal kingdom. The physics of adhesion predict that attachment is more challenging for large animals, whereas detachment is harder for small animals, due to the difference in surface-to-volume ratios. Here, we use stick insects to show that this problem is solved at both ends of the scale by linking adhesion to the applied shear force. Adhesive forces of individual insect pads, measured with perpendicular pull-offs, increased approximately in proportion to a linear pad dimension across instars. In sharp contrast, whole-body force measurements suggested area scaling of adhesion. This discrepancy is explained by the presence of shear forces during whole-body measurements, as confirmed in experiments with pads sheared prior to detachment. When we applied shear forces proportional to either pad area or body weight, pad adhesion also scaled approximately with area or mass, respectively, providing a mechanism that can compensate for the size-related loss of adhesive performance predicted by isometry. We demonstrate that the adhesion-enhancing effect of shear forces is linked to pad sliding, which increased the maximum adhesive force per area sustainable by the pads. As shear forces in natural conditions are expected to scale with mass, sliding is more frequent and extensive in large animals, thus ensuring that large animals can attach safely, while small animals can still detach their pads effortlessly. Our results therefore help to explain how nature's climbers maintain a dynamic attachment performance across seven orders of magnitude in body weight.

Porous substrate affects a subsequent attachment ability of the beetle Harmonia axyridis (Coleoptera, Coccinellidae).

According to literature data, porous substrates can cause a reduction of insect attachment ability. We carried out traction experiments with adult ladybird beetles Harmonia axyridis on the smooth solid glass sample and rough porous Al2O3 membrane to prove the primary effect of absorption of the insect pad secretion by porous media, rather than surface roughness, on the attachment force on the porous sample. With each insect individual, a set of five experiments was conducted: (1) on glass; (2) on the porous membrane; (3-5) on glass immediately after the test on the porous surface, then after 30 min and 1 h of recovery time. On the porous substrate, the forces, being similar in females and males, were greatly reduced compared to those measured on glass. A significant difference between the force values obtained in the first (before the test on the porous sample) and second (immediately after the experiment on the porous sample) tests on glass was observed. After 30 min recovery time, beetles completely regained their attachment ability. Females produced significantly lower forces than males in all experiments on glass: the differences are probably caused by the sexual dimorphism in the microstructure of their adhesive pads. The obtained results are of fundamental importance for further application in biomimetics of novel insect-repelling surfaces and in plant protection by using porous materials.

Biomechanics of shear-sensitive adhesion in climbing animals: peeling, pre-tension and sliding-induced changes in interface strength

Many arthropods and small vertebrates use adhesive pads for climbing. These biological adhesives have to meet conflicting demands: attachment must be strong and reliable, yet detachment should be fast and effortless. Climbing animals can rapidly and reversibly control their pads' adhesive strength by shear forces, but the mechanisms underlying this coupling have remained unclear. Here, we show that adhesive forces of stick insect pads closely followed the predictions from tape peeling models when shear forces were small, but strongly exceeded them when shear forces were large, resulting in an approximately linear increase of adhesion with friction. Adhesion sharply increased at peel angles less than ca 30°, allowing a rapid switch between attachment and detachment. The departure from classic peeling theory coincided with the appearance of pad sliding, which dramatically increased the peel force via a combination of two mechanisms. First, partial sliding pre-stretched the pads, so that they were effectively stiffer upon detachment and peeled increasingly like inextensible tape. Second, pad sliding reduces the thickness of the fluid layer in the contact zone, thereby increasing the stress levels required for peeling. In combination, these effects can explain the coupling between adhesion and friction that is fundamental to adhesion control across all climbing animals. Our results highlight that control of adhesion is not solely achieved by direction-dependence and morphological anisotropy, suggesting promising new routes for the development of controllable bio-inspired adhesives.

Rate-dependence of 'wet' biological adhesives and the function of the pad secretion in insects.

Many insects use soft adhesive footpads for climbing. The surface contact of these organs is mediated by small volumes of a liquid secretion, which forms thin films in the contact zone. Here, we investigate the role of viscous dissipation by this secretion and the 'bulk' pad cuticle by quantifying the rate-dependence of the adhesive force of individual pads. Adhesion increased with retraction speed, but this effect was independent of the amount of pad secretion present in the contact zone, suggesting that the secretion's viscosity did not play a significant role. Instead, the rate-dependence can be explained by relating the strain energy release rate to the speed of crack propagation, using an established empirical power law. The 'wet' pads' behaviour was akin to that of 'dry' elastomers, with an equilibrium energy release rate close to that of dry van-der-Waals contacts. We suggest that the secretion mainly serves as a 'release layer', minimising viscous dissipation and thereby reducing the time- and 'loading-history'-dependence of the adhesive pads. In contrast to many commercial adhesives which derive much of their strength from viscous dissipation, we show that the major modulator of adhesive strength in 'wet' biological adhesive pads is friction, exhibiting a much larger effect than retraction speed. A comparison between 'wet' and 'dry' biological adhesives, using both results from this study and the literature, revealed a striking lack of differences in attachment performance under varying experimental conditions. Together, these results suggest that 'wet' and 'dry' biological adhesives may be more similar than previously thought.

Adhesion force measurements on the two wax layers of the waxy zone in Nepenthes alata pitchers.

The wax coverage of the waxy zone in Nepenthes alata pitchers consists of two clearly distinguishable layers, designated the upper and lower wax layers. Since these layers were reported to reduce insect attachment, they were considered to have anti-adhesive properties. However, no reliable adhesion tests have been performed with these wax layers. In this study, pull-off force measurements were carried out on both wax layers of the N. alata pitcher and on two reference polymer surfaces using deformable polydimethylsiloxane half-spheres as probes. To explain the results obtained, roughness measurements were performed on test surfaces. Micro-morphology of both surface samples and probes tested was examined before and after experiments. Pull-off forces measured on the upper wax layer were the lowest among surfaces tested. Here, contamination of probes by wax crystals detached from the pitcher surface was found. This suggests that low insect attachment on the upper wax layer is caused primarily by the breaking off of wax crystals from the upper wax layer, which acts as a separation layer between the insect pad and the pitcher surface. High adhesion forces obtained on the lower wax layer are explained by the high deformability of probes and the particular roughness of the substrate.

Insect wet steps: loss of fluid from insect feet adhering to a substrate.

Reliable attachment ability of insect adhesive pads is proposed to be due to pad secretion. It has been shown that surface roughness strongly reduces adhesion forces of insect pads. This effect has been explained by decreased contact area and rapid fluid absorption from the pad surface by rough surfaces. However, it remains unclear how the fluid flows on rough substrates having different roughness parameters and surface energy. In this paper, we numerically studied the fluid flow on rough substrates during contact formation. The results demonstrate that an increase in the density of the substrate structures leads to an increase in fluid loss from the pad: substrates with a fine roughness absorb pad fluid faster. Decreased affinity of the solid substrate to the fluid has a more remarkable effect on the fluid loss and leads to a decrease in the fluid loss. With an increase in the aspect ratio of the substrate irregularities (porosity), the fluid loss is decreased. The numerical results obtained agree well with previous observations on insects and experimental results on nanoporous substrata. The significance of the obtained results for understanding biological wet adhesives is discussed.

Mechanisms of self-cleaning in fluid-based smooth adhesive pads of insects

Pressure-sensitive adhesives such as tapes become easily contaminated by dust particles. By contrast, animal adhesive pads are able to self-clean and can be reused millions of times over a lifetime with little reduction in adhesion. However, the detailed mechanisms underlying this ability are still unclear. Here we test in adhesive pads of stick insects (Carausius morosus) (1) whether self-cleaning is enhanced by the liquid pad secretion, and (2) whether alternating push–pull movements aid the removal of particles. We measured attachment forces of insect pads on glass after contamination with 10 µm polystyrene beads. While the amount of fluid present on the pad showed no effect on the pads' susceptibility to contamination, the recovery of adhesive forces after contamination was faster when higher fluid levels were present. However, this effect does not appear to be based on a faster rate of self-cleaning since the number of spheres deposited with each step did not increase with fluid level. Instead, the fluid may aid the recovery of adhesive forces by filling in the gaps between contaminating particles, similar to the fluid's function on rough surfaces. Further, we found no evidence that an alternation of pushing and pulling movements, as found in natural steps, leads to a more efficient recovery of adhesion than repeated pulling slides.

In vivo dynamics of the internal fibrous structure in smooth adhesive pads of insects

Many insects with smooth adhesive pads can rapidly enlarge their contact area by centripetal pulls on the legs, allowing them to cope with sudden mechanical perturbations such as gusts of wind or raindrops. The short time scale of this reaction excludes any neuromuscular control; it is thus more likely to be caused by mechanical properties of the pad’s specialized cuticle. This soft cuticle contains numerous branched fibrils oriented almost perpendicularly to the surface. Assuming a fixed volume of the water-filled cuticle, we hypothesized that pulls could decrease the fibril angle, thereby helping the contact area to expand laterally and longitudinally. Three-dimensional fluorescence microscopy on the cuticle of smooth stick insect pads confirmed that pulls significantly reduced the fibril angle. However, the fibril angle variation appeared insufficient to explain the observed increase in contact area. Direct strain measurements in the contact zone demonstrated that pulls not only expand the cuticle laterally, but also add new contact area at the pad’s outer edge.

Extensive collection of femtolitre pad secretion droplets in the beetleLeptinotarsa decemlineataallows nanolitre microrheology

Pads of beetles are covered with long, deformable setae, each ending in a micrometric terminal plate coated with secretory fluid. It was recently shown that the layer of the pad secretion covering the terminal plates is responsible for the generation of strong attractive forces. However, less is known about the fluid itself because it is produced in an extremely small quantity. We present here the first experimental investigation of the rheological properties of the pad secretion in the Colorado potato beetleLeptinotarsa decemlineata(Coleoptera, Chrysomelidae). Because the secretion is produced in an extremely small amount at the level of the terminal plate, we first developed a procedure based on capillary effects to collect the secretion for rheological experiments. In order to study the collected fluid (less than 1 nl) through passive microrheology, we managed to incorporate micrometric probes (melamine beads) that were initially in the form of a dry powder. Finally, the bead thermal motions were observed optically and recorded to determine the mechanical properties of the surrounding medium. We achieved this quantitative measurement with the collected volume, which is much smaller than the usual 1 µl sample volume required for this technique. Surprisingly, the beetle secretion was found to behave as a purely viscous liquid, of high viscosity (about 100 times that of water). This suggests that no specific complex fluid behaviour is needed by this adhesive system during beetle locomotion. We describe a scenario for the contact formation between the spatula at the setal tip and a smooth substrate, during the insect walk. We show that the attachment dynamics of the insect pad computed from the high measured viscosity is in good agreement with the observed insect pace. We finally discuss the consequences of the viscosity of the secretion on the insect adhesion.

Slippery surfaces of pitcher plants: Nepenthes wax crystals minimize insect attachment via microscopic surface roughness

Pitcher plants of the genus Nepenthes efficiently trap and retain insect prey in highly specialized leaves. Besides a slippery peristome which inhibits adhesion of insects they employ epicuticular wax crystals on the inner walls of the conductive zone of the pitchers to hamper insect attachment by adhesive devices. It has been proposed that the detachment of individual crystals and the resulting contamination of adhesive organs is responsible for capturing insects. However, our results provide evidence in favour of a different mechanism, mainly based on the stability and the roughness of the waxy surface. First, we were unable to detect a large quantity of crystal fragments on the pads of insects detached from mature pitcher surfaces of Nepenthes alata. Second, investigation of the pitcher surface by focused ion beam treatment showed that the wax crystals form a compact 3D structure. Third, atomic force microscopy of the platelet-shaped crystals revealed that the crystals are mechanically stable, rendering crystal detachment by insect pads unlikely. Fourth, the surface profile parameters of the wax layer showed striking similarities to those of polishing paper with low grain size. By measuring friction forces of insects on this artificial surface we demonstrate that microscopic roughness alone is sufficient to minimize insect attachment. A theoretical model shows that surface roughness within a certain length scale will prevent adhesion by being too rough for adhesive pads but not rough enough for claws.

Evidence for self-cleaning in fluid-based smooth and hairy adhesive systems of insects

Insects possess adhesive organs that allow attachment to diverse surfaces. Efficient adhesion must be retained throughout their lifetime even when pads are exposed to contamination. Many insects groom their adhesive structures, but it is possible that self-cleaning properties also play an important role. We measured attachment forces of insect pads on glass after contamination with microspheres and found that both smooth pads (stick insects: Carausius morosus) and hairy pads (dock beetles: Gastrophysa viridula) exhibit self-cleaning. Contaminated pads recovered high levels of adhesion after only eight simulated steps; this was accompanied by the deposition of spheres. Self-cleaning was strongly enhanced by shear movements, and only beetle pads showed the ability to self-clean during purely perpendicular pull-offs. Hairy pads also self-cleaned more efficiently than smooth pads for both large (45 microm) and small (1 microm) particle sizes. However, the beetles' self-cleaning was not superior to smooth pads when contaminated with 10-microm beads. This limitation of self-cleaning is explained by the coincidence of bead diameter and inter-seta distance, which caused beads to remain trapped in between setae.

Insect tricks: two-phasic foot pad secretion prevents slipping

Many insects cling to vertical and inverted surfaces with pads that adhere by nanometre-thin films of liquid secretion. This fluid is an emulsion, consisting of watery droplets in an oily continuous phase. The detailed function of its two-phasic nature has remained unclear. Here we show that the pad emulsion provides a mechanism that prevents insects from slipping on smooth substrates. We discovered that it is possible to manipulate the adhesive secretion in vivo using smooth polyimide substrates that selectively absorb its watery component. While thick layers of polyimide spin-coated onto glass removed all visible hydrophilic droplets, thin coatings left the emulsion in its typical form. Force measurements of stick insect pads sliding on these substrates demonstrated that the reduction of the watery phase resulted in a significant decrease in friction forces. Artificial control pads made of polydimethylsiloxane showed no difference when tested on the same substrates, confirming that the effect is caused by the insects' fluid-based adhesive system. Our findings suggest that insect adhesive pads use emulsions with non-Newtonian properties, which may have been optimized by natural selection. Emulsions as adhesive secretions combine the benefits of 'wet' adhesion and resistance against shear forces.

Comparison of smooth and hairy attachment pads in insects: friction,adhesion and mechanisms for direction-dependence

Adhesive pads on the legs of animals can be classified as either 'smooth' or 'hairy' (fibrillar). It has been proposed that the hairy design conveys superior and controllable adhesion. However, no study has yet compared the basic performance of both systems. As such, we measured single-pad friction and adhesion forces in sample hairy (Gastrophysa viridula) and smooth (Carausius morosus) pads and simultaneously recorded contact area. Adhesion and friction forces per unit pad area were very similar in smooth and hairy systems. Insect pads of both types adhere via a thin film of liquid secretion. As found previously for the smooth system, forces in the fibrillar system strongly decreased with larger amounts of fluid secretion present, suggesting that the fluid mainly serves to maximize contact on rough substrates. One essential prerequisite for the control of surface attachment during locomotion is the direction-dependence of adhesive pads. We compared the mechanisms of direction-dependence in smooth and hairy systems by performing proximal and distal slides. Both types of pad exhibited a large drop in friction when moved away from the body, although this effect was more extreme for the hairy system. Direction-dependence is explained in both smooth and fibrillar systems by the instability of the tarsal chain, causing the whole pad to peel off. In the fibrillar pads, anisotropy additionally arises from the direction-dependence of individual setae.

Impact of confined liquid thin film upon bioadhesive force between insect pads and smooth solid surface

The outstanding climbing skills on smooth solid surface of some insects like beetle, bee and cockroach or some small reptiles like gecko have been under investigation for a long time. When some kinds of insects crawl on a smooth glass surface, the micro_pads leave traces of self-secreted organic liquid, which suggests that, the thin layer of confined liquid may contribute to the bioadhesive force between the micro_pad and the smooth surface. To investigate the properties of the confined liquid thin film, a series of experiments were carried out on a home-made microtribometer with a trace amount of ionic liquid (［emim］ ［Tf2N］) or PAO(poly_α_olefin) oil confined between a nano-scale smooth steel sphere and a glass plate. For a critical confined volume of pitoliters to nanoliters, and a critical clearance of tens to hundreds of nanometers, confinement-induced spontaneous spreading and abrupt shrinking were observed, accompanied by the presence of a stable interfacial adhesive force of remarkable magnitude. This spreading/shrinking-induced adhesive force was proved to be fundamentally different from the common meniscus capillary force and was considered to stem from confinement-induced solidification, according to our further investigations. The confinement-induced adhesive force of organic liquid may shed significant light on the physical principle “employed” by insects to crawl quickly on smooth vertical surfaces. By subtly adjusting the volume of confined liquid or the clearance between the pads and the surface, insects can control (i.e., switch on or off) the interfacial force at will. The interfacial bonding force of confined liquid thin film discovered in this paper may provide a basis for the principle of biomimetic attachment systems.

An Integrative Study of Insect Adhesion: Mechanics and Wet Adhesion of Pretarsal Pads in Ants

Many animals that locomote by legs possess adhesive pads. Such organs are rapidly releasable and adhesive forces can be controlled during walking and running. This capacity results from the interaction of adhesive with complex mechanical systems. Here we present an integrative study of the mechanics and adhesion of smooth attachment pads (arolia) in Asian Weaver ants (Oecophylla smaragdina). Arolia can be unfolded and folded back with each step. They are extended either actively by contraction of the claw flexor muscle or passively when legs are pulled toward the body. Regulation of arolium use and surface attachment includes purely mechanical control inherent in the arrangement of the claw flexor system.Predictions derived from a 'wet' adhesion mechanism were tested by measuring attachment forces on a smooth surface using a centrifuge technique. Consistent with the behavior of a viscid secretion, frictional forces per unit contact area linearly increased with sliding velocity and the increment strongly decreased with temperature.We studied the nature and dimensions of the adhesive liquid film using Interference Reflection Microscopy (IRM). Analysis of 'footprint' droplets showed that they are hydrophobic and form low contact angles. In vivo IRM of insect pads in contact with glass, however, revealed that the adhesive liquid film not only consists of a hydrophobic fluid, but also of a volatile, hydrophilic phase. IRM allows estimation of the height of the liquid film and its viscosity. Preliminary data indicate that the adhesive secretion alone is insufficient to explain the observed friction and that rubbery deformation of the pad cuticle is involved.