Tarsal morphology and attachment ability of the codling moth Cydia pomonella L. (Lepidoptera, Tortricidae) to smooth surfaces

Despite several studies on the attachment ability of different insect taxa, little is known about this phenomenon in adult Lepidoptera. In this study we combined morphological and experimental analyses of tarsal adhesive devices and the attachment ability of the codling moth Cydia pomonella (L.) (Lepidoptera, Tortricidae) to smooth surfaces. Pretarsi of C. pomonella attach to smooth substrates by means of their smooth, flexible and well developed arolia. Using the centrifugal force measurement technique, friction forces of males and females were assessed on hydrophobic and hydrophilic glass surfaces. Adults of both sexes generated similar forces in spite of the noticeable difference in their body masses. That is why males showed significantly higher safety factors (attachment force divided by body weight) compared to those of females. Hydrophobicity of the substrate had no considerable effect on friction forces. For females, friction forces (sliding parallel to the substrate plane) were compared with adhesive forces (pulling off perpendicularly from the substrate plane) measured on Plexiglas surfaces. It can be concluded that the attachment system of C. pomonella is rather robust against physico-chemical properties of the substrate and is able to achieve a very good attachment on vertical and horizontal substrata.     

Biomechanics of smooth adhesive pads in insects: influence of tarsal secretion on attachment performance

Many insects possess smooth adhesive pads on their legs, which adhere by thin films of a two-phasic secretion. To understand the function of such fluid-based adhesive systems, we simultaneously measured adhesion, friction and contact area in single pads of stick insects (Carausius morosus). Shear stress was largely independent of normal force and increased with velocity, seemingly consistent with the viscosity-effect of a continuous fluid film. However, measurements of the remaining force 2 min after a sliding movement show that adhesive pads can sustain considerable static friction. Repeated sliding movements and multiple consecutive pull-offs to deplete adhesive secretion showed that on a smooth surface, friction and adhesion strongly increased with decreasing amount of fluid. In contrast, pull-off forces significantly decreased on a rough substrate. Thus, the secretion does not generally increase attachment but does so only on rough substrates, where it helps to maximize contact area. When slides were repeated at one position so that secretion could accumulate, sliding shear stress decreased but static friction remained clearly present. This suggests that static friction which is biologically important to prevent sliding is based on non-Newtonian properties of the adhesive emulsion rather than on a direct contact between the cuticle and the substrate.     

Attachment ability of sawfly larvae to smooth surfaces

Larvae of the sawfly Rhadinoceraea micans adhere properly to the anti-adhesive surface of their host plant Iris pseudacorus by using three pairs of thoracic legs, seven pairs of abdominal prolegs, and pygopodia, all provided with various smooth adhesive pads. Their attachment performance to smooth flat hydrophilic and hydrophobic glass and Plexiglas surfaces was studied in centrifugal force experiments. Obtained safety factors on Plexiglas were up to 25 in friction, and 8 in adhesion. Although larvae attached significantly stronger to the hydrophilic glass, they attached well also to the hydrophobic one. Pygopodia are suggested to dominate attachment force generation in the centrifugal force experiment. Transverse body position on the centrifuge drum was significantly advantageous for friction force generation than was longitudinal body position. Results are discussed in the context of the sawfly biology and provide a profound base for further detailed studies on biomechanics of sawfly larvae–plant interactions.     

An integrative study of insect adhesion: mechanics and wet adhesion of pretarsal pads in ants

Many animals that locomote by legs possess adhesive pads. Suchorgans are rapidly releasable and adhesive forces can be controlledduring walking and running. This capacity results from the interactionof adhesive with complex mechanical systems. Here we presentan integrative study of the mechanics and adhesion of smoothattachment pads (arolia) in Asian Weaver ants (Oecophylla smaragdina).Arolia can be unfolded and folded back with each step. Theyare extended either actively by contraction of the claw flexormuscle or passively when legs are pulled toward the body. Regulationof arolium use and surface attachment includes purely mechanicalcontrol inherent in the arrangement of the claw flexor system. Predictions derived from a ‘wet’ adhesion mechanismwere tested by measuring attachment forces on a smooth surfaceusing a centrifuge technique. Consistent with the behavior ofa viscid secretion, frictional forces per unit contact arealinearly increased with sliding velocity and the increment stronglydecreased with temperature. We studied the nature and dimensions of the adhesive liquidfilm using Interference Reflection Microscopy (IRM). Analysisof ‘footprint’ droplets showed that they are hydrophobicand form low contact angles. In vivo IRM of insect pads in contactwith glass, however, revealed that the adhesive liquid filmnot only consists of a hydrophobic fluid, but also of a volatile,hydrophilic phase. IRM allows estimation of the height of theliquid film and its viscosity. Preliminary data indicate thatthe adhesive secretion alone is insufficient to explain theobserved friction and that rubbery deformation of the pad cuticleis involved.     

Sexual dimorphism in the attachment ability of the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) to rough substrates

Many representatives of the beetle family Chrysomelidae exhibit a distinctive sexual dimorphism in the structure of adhesive tarsal setae. The present study demonstrates the influence of surface roughness on the friction force of Leptinotarsa decemlineata males and females. The maximum friction force of individual beetles was measured on epoxy resin surfaces (smooth and with asperities ranging from 0.3 to 12.0 microm) using a centrifugal force tester. On the smooth surface, no considerable differences between males and females were found, whereas on rough surfaces, females attached significantly (up to two times) stronger than males. Clawless beetles generated lower forces than intact ones, but demonstrated similar differences between males and females. The results indicate that the female adhesive system has its main functional trait in a stronger specialisation to rough plant surfaces whereas the adhesive system of males possess a certain trade-off between attachment to rough plant surfaces during locomotion on vegetation and to the smooth surface of the female elytra, while mating.     

Attachment ability of the codling moth Cydia pomonella L. to rough substrates

Host plant surfaces of the codling moth, Cydia pomonella L. (Lepidoptera, Tortricidae), vary in microtopography, which can affect its attachment, locomotion, and oviposition behaviour. This study was performed to investigate the effect of surface roughness on the attachment ability of adult insects. Using a centrifugal force device, friction forces of both sexes were assessed on six epoxy resin substrates differing only in the dimensions of their surface asperities, ranging from 0 μm to 12 μm. Surface topography significantly affected friction forces. Maximal force was measured on the smooth substrate whereas minimal force was assessed on microrough substrates with 0.3 μm and 1.0 μm size of asperities. On the remaining rough substrates, friction forces were significantly higher but still lower than on the smooth substrate. Both sexes generated similar forces on the same substrate, in spite of the considerable difference in their body mass. Thus, it is expected that both sexes can attach effectively to differently structured plant substrates in their habitat. However, since smooth surfaces have been reported previously to be the most favorable substrates for ovipositing females of C. pomonella, it is possible that they use their attachment system to sense the substrate texture and prefer those substrates to which their arolia attach the best.     

Functionally Different Pads on the Same Foot Allow Control of Attachment: Stick Insects Have Load-Sensitive “Heel” Pads for Friction and Shear-Sensitive “Toe” Pads for Adhesion

Stick insects (Carausius morosus) have two distinct types of attachment pad per leg, tarsal “heel” pads (euplantulae) and a pre-tarsal “toe” pad (arolium). Here we show that these two pad types are specialised for fundamentally different functions. When standing upright, stick insects rested on their proximal euplantulae, while arolia were the only pads in surface contact when hanging upside down. Single-pad force measurements showed that the adhesion of euplantulae was extremely small, but friction forces strongly increased with normal load and coefficients of friction were 1. The pre-tarsal arolium, in contrast, generated adhesion that strongly increased with pulling forces, allowing adhesion to be activated and deactivated by shear forces, which can be produced actively, or passively as a result of the insects'' sprawled posture. The shear-sensitivity of the arolium was present even when corrected for contact area, and was independent of normal preloads covering nearly an order of magnitude. Attachment of both heel and toe pads is thus activated partly by the forces that arise passively in the situations in which they are used by the insects, ensuring safe attachment. Our results suggest that stick insect euplantulae are specialised “friction pads” that produce traction when pressed against the substrate, while arolia are “true” adhesive pads that stick to the substrate when activated by pulling forces.     

In the footsteps of sea stars: deciphering the catalogue of proteins involved in underwater temporary adhesion

Sea stars adhere strongly but temporarily to underwater substrata via the secretion of a blend of proteins, forming an adhesive footprint that they leave on the surface after detachment. Their tube feet enclose a duo-gland adhesive system comprising two types of adhesive cells, contributing different layers of the footprint and de-adhesive cells. In this study, we characterized the catalogue of sea star footprint proteins (Sfps) in the species Asterias rubens to gain insights in their potential function. We identified 16 Sfps and mapped their expression to type 1 and/or type 2 adhesive cells or to de-adhesive cells by double fluorescent in situ hybridization. Based on their cellular expression pattern and their conserved functional domains, we propose that the identified Sfps serve different functions during attachment, with two Sfps coupling to the surface, six providing cohesive strength and the rest forming a binding matrix. Immunolabelling of footprints with antibodies directed against one protein of each category confirmed these roles. A de-adhesive gland cell-specific astacin-like proteinase presumably weakens the bond between the adhesive material and the tube foot surface during detachment. Overall, we provide a model for temporary adhesion in sea stars, including a comprehensive list of the proteins involved.     

Friction force reduction triggers feet grooming behaviour in beetles

In insects, cleaning (grooming) of tarsal attachment devices is essential for maintaining their adhesive ability, necessary for walking on a complex terrain of plant surfaces. How insects obtain information on the degree of contamination of their feet has remained, until recently, unclear. We carried out friction force measurements on walking beetles Gastrophysa viridula (Coleoptera, Chrysomelidae) and counted grooming occurrence on stiff polymer substrata with different degrees of nanoroughness (root mean square: 28-288 nm). Since nanoscopically, rough surfaces strongly reduced friction and adhesion without contaminating feet, we were able to demonstrate, for the first time to our knowledge, that friction force between tarsal attachment pads and the substrate provides an insect with information on the degree of contamination of its attachment structures. We have shown that foot grooming occurrence correlates not only with the degree of contamination but also with the decrease of friction force. This result indicates that insects obtain information about the degree of contamination, not statically but rather dynamically and, presumably, use mechanoreceptors monitoring either tensile/compressive forces in the cuticle or tensile forces between leg segments.     

Effect of Microscale Contact State of Polyurethane Surface on Adhesion and Friction

The effect of microscale contact of rough surfaces on the adhesion and friction under negative normal forces was experimentally investigated. The adhesive force of single point contact - sapphire ball to flat polyurethane did not vary with the normal force. With rough surface contact, which was assumed to be a great number of point contacts, the adhesive force increased logarithmically with the normal force. Under negative normal force adhesive state, the tangential force （more than hundred mN） were much larger than the negative normal force （several mN） and increased with the linear decrease of negative normal force. The results reveal why the gecko＇s toe must slide slightly on the target surface when it makes contact on a surface and suggest how a biomimetic gecko foot might be designed.     

Arachnids secrete a fluid over their adhesive pads

Background

Many arachnids possess adhesive pads on their feet that help them climb smooth surfaces and capture prey. Spider and gecko adhesives have converged on a branched, hairy structure, which theoretically allows them to adhere solely by dry (solid-solid) intermolecular interactions. Indeed, the consensus in the literature is that spiders and their smooth-padded relatives, the solifugids, adhere without the aid of a secretion.

Methodology and Principal Findings

We investigated the adhesive contact zone of living spiders, solifugids and mites using interference reflection microscopy, which allows the detection of thin liquid films. Like insects, all the arachnids we studied left behind hydrophobic fluid footprints on glass (mean refractive index: 1.48–1.50; contact angle: 3.7–11.2°). Fluid was not always secreted continuously, suggesting that pads can function in both wet and dry modes. We measured the attachment forces of single adhesive setae from tarantulas (Grammostola rosea) by attaching them to a bending beam with a known spring constant and filming the resulting deflection. Individual spider setae showed a lower static friction at rest (26%±2.8 SE of the peak friction) than single gecko setae (Thecadactylus rapicauda; 96%±1.7 SE). This may be explained by the fact that spider setae continued to release fluid after isolation from the animal, lubricating the contact zone.

Significance

This finding implies that tarsal secretions occur within all major groups of terrestrial arthropods with adhesive pads. The presence of liquid in an adhesive contact zone has important consequences for attachment performance, improving adhesion to rough surfaces and introducing rate-dependent effects. Our results leave geckos and anoles as the only known representatives of truly dry adhesive pads in nature. Engineers seeking biological inspiration for synthetic adhesives should consider whether model species with fluid secretions are appropriate to their design goals.     

High resolution characterization of ectomycorrhizal fungal-mineral interactions in axenic microcosm experiments

Microcosms with Pinus sylvestris seedlings in symbiosis with the fungus mycorrhizal Paxillus involutus were established, and atomic force microscopy (AFM) was used to characterise plant photosynthate-driven fungal interactions with mineral surfaces. Comparison of images of the same area of the minerals before and after mycorrhizal fungal colonization showed extensive growth of hyphae on three different mineral surfaces – hornblende, biotite and chlorite. A layer of biological exudate, or biolayer, covered the entire mineral surface and was composed of globular features of diameter 10–80 nm, and the morphology of the biolayer differed among mineral types. Similar-sized components were found on the fungal hyphae, but with a more elongated profile. Biolayer and hyphae surfaces both appeared to be hydrophobic with the hyphal surfaces yielding higher maximal adhesive interactions and a wider range of values: the mean (± SE) adhesive forces were 2.63 ± 0.03 and 3.46 ± 0.18 nN for biolayer and hypha, respectively. The highest adhesion forces are preferentially localized at the hyphal surface above the Spitzenkörper region and close to the tip, with a mean interaction force in this locality of 5.24 ± 0.49 nN. Biolayer thickness was between 10 and 40 nm. The underlying mineral was easily broken up by the tip, in contrast to the native mineral. These observations of mineral surfaces colonised by mycorrhizal fungus demonstrate how fungal hyphae are able to form a layer of organic exudates, or biolayer, and its role in hyphal attachment and potential weathering of ferromagnesian silicates, which may supply nutrients to the plant.     

螽斯吸附足垫的构造及其吸附性能分析

许多昆虫足上有光滑吸附垫,通过二相分泌液粘附到各种表面。为理解这种基于液体的吸附系统的功能,用在螽斯身上绑细线的方法,测量其在不同表面的摩擦力和吸附力,并用高速摄像机观察足垫的构造及吸附和分离的动作,测试足垫与接触面的接触面积。结果表明螽斯的水平摩擦力大于垂直吸附力。足垫与表面接触时向身体方向拖动来增加摩擦力。分离时采用剥离的方法,但剥离方向与刚毛型足垫的相反,是从末梢端翘起分离,达到行动迅速且节省能量的目的。测试结果可用于机器人吸附足掌的仿生设计。     

Interaction of liquid epicuticular hydrocarbons and tarsal adhesive secretion in Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae)

Species of various insect orders possess specialised tarsal adhesive structures covered by a thin liquid film, which is deposited in the form of footprints. This adhesive liquid has been suggested to be chemically and physiologically related to the epicuticular lipid layer, which naturally covers the body of insects and acts as the prime barrier to environmental stresses, such as desiccation. The functional efficiency of the layer, however, is jeopardised by partial melting that may occur at physiological temperatures. In this study, light microscopic images of elytral prints show that the epicuticular lipid layer of the Colorado potato beetle Leptinotarsa decemlineata actually is partially liquid and chemical investigations reveal the high similarity of the epicuticular hydrocarbon pattern and the tarsal liquid. By means of chemical manipulation of the surface hydrocarbon composition of live beetles, the substance exchange between their tarsal adhesive hairs and the body surface is monitored. Histological sections of L. decemlineata tarsi, furthermore, reveal glandular cells connected to individual adhesive setae and departing from these results, an idea of a general mechanism of tarsal secretion is developed and discussed in a functional–ecological context.     

Adhesion forces measured at the level of a terminal plate of the fly's seta

The attachment pads of fly legs are covered with setae, each ending in small terminal plates coated with secretory fluid. A cluster of these terminal plates contacting a substrate surface generates strong attractive forces that hold the insect on smooth surfaces. Previous research assumed that cohesive forces and molecular adhesion were involved in the fly attachment mechanism. The main elements that contribute to the overall attachment force, however, remained unknown. Multiple local force-volume measurements were performed on individual terminal plates by using atomic force microscopy. It was shown that the geometry of a single terminal plate had a higher border and considerably lower centre. Local adhesion was approximately twice as strong in the centre of the plate as on its border. Adhesion of fly footprints on a glass surface, recorded within 20 min after preparation, was similar to adhesion in the centre of a single attachment pad. Adhesion strongly decreased with decreasing volume of footprint fluid, indicating that the layer of pad secretion covering the terminal plates is crucial for the generation of a strong attractive force. Our data provide the first direct evidence that, in addition to Van der Waals and Coulomb forces, attractive capillary forces, mediated by pad secretion, are a critical factor in the fly's attachment mechanism.     

Adhesive and frictional properties of tarsal attachment pads in two species of stick insects (Phasmatodea) with smooth and nubby euplantulae

In the present study, the tarsal attachment pads (euplantulae) of two stick insect species (Phasmatodea) were compared. While the euplantulae of Cuniculina impigra (syn. Medauroidea extradentata) are smooth, those of Carausius morosus bear small nubs on their surfaces. In order to characterize the adhesive and frictional properties of both types of euplantulae, adhesion and friction measurements on smooth (Ra=0.054 μm) and rough (Ra=1.399 μm) substrates were carried out. The smooth pads of C. impigra generated stronger adhesion on the smooth substrate than on the rough one. The adhesive forces of the structured pads of C. morosus did not differ between the two substrates. Friction experiments showed anisotropy for both species with higher values for proximal pulls than for distal pushes. In C. impigra, friction was stronger on the smooth than on the rough surface for both directions, whereas in C. morosus friction was stronger on the smooth surface only for pushes. This shows that smooth attachment pads are able to generate relatively stronger adhesion and friction on a flat smooth surface than on a rough one. In contrast, nubby pads have similar adhesion on both substrates, and also show no difference in friction in the pulling direction. This leads to the conclusion that smooth pads are specialized for rather smooth substrates, whereas nubby pads are better adapted to generate stronger forces on a broader range of surfaces.     

Predicting the chemical composition and structure of Aspergillus nidulans hyphal wall surface by atomic force microscopy

In fungi, cell wall plays an important role in growth and development. Major macromolecular constituents of the aspergilli cell wall are glucan, chitin, and protein. We examined the chemical composition and structure of the Aspergillus nidulans hyphal wall surface by an atomic force microscope (AFM). To determine the composition of the cell wall surface, the adhesion forces of commercially available β-glucan, chitin, and various proteins were compared to those of corresponding fractions prepared from the hyphal wall. In both setups, the adhesion forces of β-glucan, chitin, and protein were 25–50, 1000–3000, and 125–300 nN, respectively. Adhesion force analysis demonstrated that the cell surface of the apical tip region might contain primarily chitin and β-glucan and relatively a little protein. This analysis also showed the chemical composition of the hyphal surface of the mid-region would be different from that of the apical region. Morphological images obtained by the tapping mode of AFM revealed that the hyphal tip surface has moderate roughness.     

Finite element sub-modeling analyses of damage to enamel at the incisor enamel/adhesive interface upon de-bonding for different orthodontic bracket bases

This study investigates the micro-mechanical behavior associated with enamel damage at an enamel/adhesive interface for different bracket bases subjected to various detachment forces using 3-D finite element (FE) sub-modeling analysis. Two FE macro-models using triangular and square bracket bases subjected to shear, tensile and torsional de-bonding forces were established using μCT images. Six enamel/adhesive interface sub-models with micro- resin tag morphology and enamel rod arrangement were constructed at the corresponding stress concentrations in macro-model results. The boundary conditions for the sub-models were determined from the macro-model results and applied in sub-modeling analysis. The enamel and resin cement stress concentrations for triangular and square bases were observed at the adhesive bottom towards the occlusal surface under shear force and at the mesial and distal side planes under tensile force. The corresponding areas under torsional force were at the three corners of the adhesive for the triangular base and at the adhesive bottom toward/off the occlusal surface for the square base. In the sub-model analysis, the concentration regions were at the resin tag base and in the region around the etched holes in the enamel. These were perfectly consistent with morphological observations in a parallel in vitro bracket detachment experiment. The critical de-bonding forces damaging the enamel for the square base were lower than those of the triangular base for all detached forces. This study establishes that FE sub-modeling can be used to simulate the stress pattern at the micro-scale enamel/adhesive interface, suggesting that a square base bracket might be better than a triangular bracket. A de-bonding shear force can detach a bracket more easily than any other force with a lower risk of enamel loss.     

Is the adhesive material secreted by sea urchin tube feet species‐specific?

Sea urchin adoral tube feet are highly specialized organs that have evolved to provide efficient attachment to the substratum. They consist of a disk and a stem that together form a functional unit. Tube foot disk tenacity (adhesive force per unit area) and stem mechanical properties (e.g., stiffness) vary between species but are apparently not correlated with sea urchin taxa or habitats. Moreover, ultrastructural studies of sea urchin disk epidermis pointed out differences in the internal organization of the adhesive secretory granules among species. This prompted us to look for interspecific variability in the composition of echinoid adhesive secretions, which could explain the observed variability in adhesive granule ultrastructure and disk tenacity. Antisera raised against the footprint material of Sphaerechinus granularis (S. granularis) were first used to locate the origin of adhesive footprint constituents in tube feet by taking advantage of the polyclonal character of the generated antibodies. Immunohistochemical assays showed that the antibodies specifically labeled the adhesive secretory cells of the disk epidermis in the tube feet of S. granularis. The antibodies were then used on tube foot histological sections from seven other sea urchin species to shed some light on the variability of their adhesive substances by looking for antibody cross‐reactivity. Surprisingly, no labeling was observed in any of the species tested. These results indicate that unlike the adhesive secretions of asteroids, those of echinoids do not share common epitopes on their constituents and thus would be “species‐specific.” In sea urchins, variations in the composition of adhesive secretions could therefore explain interspecific differences in disk tenacity and in adhesive granule ultrastructure. J. Morphol., 2011. © 2011 Wiley Periodicals, Inc.     

Velocity of myosin-based actin sliding depends on attachment and detachment kinetics and reaches a maximum when myosin-binding sites on actin saturate

Molecular motors such as kinesin and myosin often work in groups to generate the directed movements and forces critical for many biological processes. Although much is known about how individual motors generate force and movement, surprisingly, little is known about the mechanisms underlying the macroscopic mechanics generated by multiple motors. For example, the observation that a saturating number, N, of myosin heads move an actin filament at a rate that is influenced by actin–myosin attachment and detachment kinetics is accounted for neither experimentally nor theoretically. To better understand the emergent mechanics of actin–myosin mechanochemistry, we use an in vitro motility assay to measure and correlate the N-dependence of actin sliding velocities, actin-activated ATPase activity, force generation against a mechanical load, and the calcium sensitivity of thin filament velocities. Our results show that both velocity and ATPase activity are strain dependent and that velocity becomes maximized with the saturation of myosin-binding sites on actin at a value that is 40% dependent on attachment kinetics and 60% dependent on detachment kinetics. These results support a chemical thermodynamic model for ensemble motor mechanochemistry and imply molecularly explicit mechanisms within this framework, challenging the assumption of independent force generation.