Microstructure of the tarsal attachment devices in the earwig Timomenus komarovi

The biological attachment device on the tarsal appendage of the earwig, Timomenus komarovi (Insecta: Dermaptera: Forficulidae) was investigated using field emission scanning electron microscopy to reveal the fine structural characteristics of its biological attachment devices to move on smooth and rough surfaces. They attach to rough substrates using their pretarsal claws; however, attachment to smooth surfaces is achieved by means of two groups of hairy tarsal pads. This biological attachment device consists of fine hairy setae with various contact sizes. Three different groups of tenent setae were distinguished depending on the cuticular substructure of the endplates. Two groups of setae commonly had flattened surfaces, and they were covered with either spoon‐shaped or spatula‐shaped endplates, respectively. While the flattened tip setae were distributed at the central region, the pointed tip setae were characteristically found along the marginal region. There were no obvious gender‐specific differences between fibrillar adhesive pads in this insect mainly because the forceps‐like pincers are used during copulation to grasp the partner.     

Fine structural analysis of the fibrillar adhesion apparatus in ladybird beetle

The attachment system on the ladybird beetle Harmonia axyridis is composed of a pair of pretarsal claws and adhesive pads at the tarsal segments. The claws, which are connected to the pretarsal segment, are mainly used to hold the rough substrates by their apical diverged hooks. In contrast, the adhesive pads have an adhesive function when landing on smooth surfaces. They are interspersed at the ventral adhesive pad of each tarsomere, and are composed of two kinds of hairy setae. The discoid tip seta (DtS) is located at the central region of each adhesive pad. The DtS has a spoon‐shaped endplate with a long and narrow shaft. In contrast, the pointed tip seta (PtS) is interspersed along the marginal regions of each adhesive pad, and has a hook‐shaped spine near the tip. In the present study, we found numerous fine cuticular pores beneath the setae, which seem to be related to the secretion of some adhesive fluids. It may be deduced that ladybird beetles can attach to smooth surfaces more effectively by employing adhesive fluids filling in surface crevices to overcome problems cause by their larger size endplates.     

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.     

Microstructure of pretarsal pulvilli in shield bug Acanthosoma spinicolle (Heteroptera: Acanthosomatidae)

Shield bugs effectively attach themselves on both rough and smooth surfaces, but their advanced biological attachment devices have not been studied closely. Our fine structural examination of the attachment devices in the shield bug A. spinicolle reveals a unique system to achieve extraordinary adhesion that allows vertical climbing. Each appendage has a pair of tarsal claws that attach to rough substrates and a pair of pretarsal pulvilli that attach to smooth surfaces. Similar to other heteropteran insects, the pulvilli of this bug are categorized as a wet adhesion system, which makes use of an adhesive fluid from the pad secretion. However, this deformable pad creates a regular pattern of contact with the mating surface with a compact array of microfolds and setae with filamentous distal protrusions. To date, this distinctive microstructure in pulvilli pads has never been reported. These microstructural characteristics should be further studied to understand biological adhesion as well as create biomimetic applications.     

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.     

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.     

Attachment ability of the beetle Chrysolina fastuosa on various plant surfaces

To study the role of different structures of a plant surface preventing insect attachment, a variety of plant surfaces were screened. Attachment ability of the beetle Chrysolina fastuosa Scop. (Coleoptera, Chrysomelidae) was measured on 99 surfaces among them smooth, hairy, felt-like, waxy, and glandular ones of three plant organs (stems, leaves, fruits) of 83 plant species belonging to 45 families. Insects attached successfully to smooth, hairy, and felt-like substrata. These surface types did not effect the further attachment of C. fastuosa, indicating the adhesive system remained intact after contacting these substrata. However, the beetles could not attach properly to surfaces covered with wax crystalloids or glandular hairs. In most experiments on pruinose plant substrata, no influence of the surfaces on the subsequent attachment ability of insects was observed. Only in one case (the stem of Acer negundo), was such an impairment recorded, but recovery of attachment ability was fast. Crystalloids of this plant species probably temporarily disable function of tenent setae of C. fastuosa. Four hypotheses, explaining anti-adhesive properties of plant surfaces, covered with wax crystalloids are proposed. A plant surface with glandular trichomes disabled the attachment system of the beetle for a long time. Secretions of trichomes probably glue tenent setae together making further attachment impossible.     

Two functional types of attachment pads on a single foot in the Namibia bush cricket Acanthoproctus diadematus (Orthoptera: Tettigoniidae)

Insects have developed different structures to adhere to surfaces. Most common are smooth and hairy attachment pads, while nubby pads have also been described for representatives of Mantophasmatodea, Phasmida and Plecoptera. Here we report on the unusual combination of nubby and smooth tarsal attachment structures in the !nara cricket Acanthoproctus diadematus. Their three proximal tarsal pads (euplantulae) have a nubby surface, whereas the most distal euplantula is rather smooth with a hexagonal ground pattern resembling that described for the great green bush-cricket Tettigonia viridissima. This is, to our knowledge, the first report on nubby euplantulae in Orthoptera and the co-occurrence of nubby and smooth euplantulae on a single tarsus in a polyneopteran species. When adhering upside down to a horizontal glass plate, A. diadematus attaches its nubby euplantulae less often, compared to situations in which the animal is hanging upright or head down on a vertical plate. We discuss possible reasons for this kind of clinging behaviour, such as morphological constrains, the different role of normal and shear forces in attachment enhancement of the nubby and smooth pads, ease of the detachment process, and adaptations to walking on cylindrical substrates.     

Gripping ease in southern green stink bugs Nezara viridula L. (Heteroptera: Pentatomidae): Coping with geometry,orientation and surface wettability of substrate

The southern green stink bug Nezara viridula L. (Heteroptera, Pentatomidae) is highly polyphagous, preferring apically situated seeds and fruits on more than 150 plant species belonging to over 30 plant families all over the world. This forces them to move over highly variable terrains, including plant stems, leaves, pods and buds, which requires efficient attachment. Stink bugs have long slender legs and feet (tarsi) equipped with paired curved claws, paired soft adhesive pads (pulvilli), and flattened lanceolate hairs (setae), which arise ventrally on the first and second foot segments (tarsomeres). To characterize their attachment abilities on well‐defined test substrates, here we comparatively measured and analyzed the traction forces of bugs walking horizontally and vertically on hydrophilic (water attractive) and hydrophobic (water repellent) glass plates and rods. The latter correspond to the geometry of preferred feeding sites of stink bugs in the field. The results show a clear contribution of tarsal flattened lanceolate hairs to the stink bug's attachment. Higher traction forces are generated on a glass rod than on a glass plate, corresponding to up to individual maximum of 43 times the stink bug's body weight. Substrate hydrophobicity promotes the attachment, while the measured forces are up to eight times lower when tarsal hairs are disabled. The combination of smooth and hairy tarsal pads results in a remarkable attachment ability, which enables N. viridula to climb unstable apical plant parts, and supports their invasive behavior and global dispersion.     

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.     

Giant stick insects reveal unique ontogenetic changes in biological attachment devices

A strong modification of tarsal and pretarsal attachment pads during the postembryonic development is described for the first time. In the exceptionally large thorny devil stick insect Eurycantha calcarata a functional arolium is only present in the immature instars, enabling them to climb on smooth surfaces, especially leaves. Nymphs are also characterized by greyish and hairy euplantulae on tarsomeres 1–4. The gradual modifications of the arolium and the euplantula of tarsomere 5 in the nymphal development are probably mainly related to increased weight. The distinct switch in the life style between the leaf-dwelling nymphal stages and the ground-dwelling adults results in the final abrupt change of the adhesive devices, resulting in a far-reaching reduction of the arolium, the presence of a fully-developed, elongated euplantula on tarsomere 5, and white and smooth euplantulae on tarsomeres 1–4. The developmental remodelling of attachment pads also reflects a phylogenetic pattern. The attachment devices of the earlier instars are similar to those found in the basalmost lineage of extant stick insects, Timema, which is characterized by a very large pan-shaped arolium and a hairy surface of the tarsal and pretarsal attachment pads.     

Underwater locomotion in a terrestrial beetle: combination of surface de-wetting and capillary forces

For the first time, we report the remarkable ability of the terrestrial leaf beetle Gastrophysa viridula to walk on solid substrates under water. These beetles have adhesive setae on their feet that produce a secretory fluid having a crucial role in adhesion on land. In air, adhesion is produced by capillary forces between the fluid-covered setae and the substrate. In general, capillary forces do not contribute to adhesion under water. However, our observations showed that these beetles may use air bubbles trapped between their adhesive setae to walk on flooded, inclined substrata or even under water. Beetle adhesion to hydrophilic surfaces under water was lower than that in air, whereas adhesion to hydrophobic surfaces under water was comparable to that in air. Oil-covered hairy pads had a pinning effect, retaining the air bubbles on their feet. Bubbles in contact with the hydrophobic substrate de-wetted the substrate and produced capillary adhesion. Additional capillary forces are generated by the pad's liquid bridges between the foot and the substrate. Inspired by this idea, we designed an artificial silicone polymer structure with underwater adhesive properties.     

On Heels and Toes: How Ants Climb with Adhesive Pads and Tarsal Friction Hair Arrays

Ants are able to climb effortlessly on vertical and inverted smooth surfaces. When climbing, their feet touch the substrate not only with their pretarsal adhesive pads but also with dense arrays of fine hairs on the ventral side of the 3^rd and 4^th tarsal segments. To understand what role these different attachment structures play during locomotion, we analysed leg kinematics and recorded single-leg ground reaction forces in Weaver ants (Oecophylla smaragdina) climbing vertically on a smooth glass substrate. We found that the ants engaged different attachment structures depending on whether their feet were above or below their Centre of Mass (CoM). Legs above the CoM pulled and engaged the arolia (‘toes’), whereas legs below the CoM pushed with the 3^rd and 4^th tarsomeres (‘heels’) in surface contact. Legs above the CoM carried a significantly larger proportion of the body weight than legs below the CoM. Force measurements on individual ant tarsi showed that friction increased with normal load as a result of the bending and increasing side contact of the tarsal hairs. On a rough sandpaper substrate, the tarsal hairs generated higher friction forces in the pushing than in the pulling direction, whereas the reverse effect was found on the smooth substrate. When the tarsal hairs were pushed, buckling was observed for forces exceeding the shear forces found in climbing ants. Adhesion forces were small but not negligible, and higher on the smooth substrate. Our results indicate that the dense tarsal hair arrays produce friction forces when pressed against the substrate, and help the ants to push outwards during horizontal and vertical walking.     

昆虫足的附着机制

昆虫卓越的爬行和附着能力来源于其精细的功能性黏附系统。根据形态结构的不同,昆虫的黏附系统可分为光滑型黏附垫和刚毛型黏附垫两种类型,二者在分泌液的支持下均能附着于几乎所有的光滑或粗糙的物体表面,而且这两种类型的黏附垫与界面的附着的形成均主要依赖于范德华力。本文综述了昆虫足的附着机制,包括光滑型和刚毛型两种黏附垫的结构和其形成附着的机理,以及黏附垫分泌液的功能、组成成分和释放机制,阐明了昆虫如何巧妙地解决稳定附着和快速脱附这一矛盾的问题,讨论了诸如界面的理化性质和环境湿度等环境因素对昆虫附着的影响,以期帮助人们深入地理解昆虫足的附着机制,并为其在仿生学等方面的应用提供理论依据。     

A scanning electron microscope study of tarsal adhesive setae in the Coleoptera

Scanning electron micrographs of the tarsal adhesive setae of 84 species of beetle are described. These show a vast range of setal structure and distribution.     

Inter- and intrasexual dimorphism in the diving beetle Hydroporus memnonius Nicolai (Coleoptera: Dytiscidae)

Sexual conflict can drive rapid intersexual arms races, and lead to pronounced sexual dimorphism. Such dimorphism is frequent in diving beetles, where males typically possess expanded front and middle tarsi, supplied with adhesive setae to grasp females during mating, and females often have rough dorsal surfaces which hinder male attachment. In a number of species, females are dimorphic, being either smooth and male-like, or heavily sculptured dorsally. Smooth and sculptured females often have distinct biogeographies, and may be expected to be associated with specific counter-adaptations in males. The European diving beetle, Hydroporus memnonius Nicolai, includes a smooth male-like female, and a matt morph, var. castaneus Aubé, which are largely allopatric in distribution. We show that the two morphs differ in the density and intensity of their surface microreticulation, and that matt females are associated with morphologically distinct males, which have developed specific countermeasures on their tarsi, including a greater number of large adhesive setae, individually larger in area. Such males are expected to be more successful in pairing with both matt and shining females, and it is suggested that a process of population replacement, partly driven by sexual interactions, may occur where the two forms overlap in range.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 685–697.     

昆虫足的吸附机制

自然界中有许多昆虫足上都有吸附垫,这些垫子经过进化能吸附在各种表面上,并能在运动中控制吸附力。昆虫吸附垫要么是光滑的表皮垫子,要么是密布特殊的刚毛。昆虫这种“飞檐走壁”的能力来自于粘液、复杂机械系统以及生物系统之间的相互作用。文章主要参考国内外研究昆虫吸附机制的文献,综述了能在光滑表面上行走的昆虫的基本爬行原理,对其吸附机制进行了分类。并分析目前研究的主要内容,提出目前昆虫吸附机制要解决的问题。最后对吸附机制在仿生机械应用上作了展望。     

Contact behaviour of tenent setae in attachment pads of the blowfly Calliphora vicina (Diptera, Calliphoridae)

To enable strong attachment forces between pad and substrata, a high proximity between contacting surfaces is required. One of the mechanisms, which can provide an intimate contact of solids, is a high flexibility of both materials. It has been previously presumed that setae of hairy attachment pads of insects are composed of flexible cuticle, and are able to replicate the surface profile. The aim of this work was to visualise the contact behaviour of the setae by freezing-substitution technique to understand setal mechanics while adhering to a smooth surface. This approach revealed considerable differences in the area of the setal tips between contacting and non-contacting pulvilli. Based on the assumption that setae behave like a spring pushed by the tip, a spring constant of 1.31 N m(-1) was calculated from direct measurements of single setae by atomic force microscopy. In order to explain the relationship between the behaviour of the attachment setae at a microscale and leg movements, high-speed video recordings were made of walking flies. This data show that some proximal movement of the leg is present during contact formation with the substrate.