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.     

Friction ridges in cockroach climbing pads: anisotropy of shear stress measured on transparent,microstructured substrates

The contact of adhesive structures to rough surfaces has been difficult to investigate as rough surfaces are usually irregular and opaque. Here we use transparent, microstructured surfaces to investigate the performance of tarsal euplantulae in cockroaches (Nauphoeta cinerea). These pads are mainly used for generating pushing forces away from the body. Despite this biological function, shear stress (force per unit area) measurements in immobilized pads showed no significant difference between pushing and pulling on smooth surfaces and on 1-μm high microstructured substrates, where pads made full contact. In contrast, on 4-μm high microstructured substrates, where pads made contact only to the top of the microstructures, shear stress was maximal during a push. This specific direction dependence is explained by the interlocking of the microstructures with nanometre-sized “friction ridges” on the euplantulae. Scanning electron microscopy and atomic force microscopy revealed that these ridges are anisotropic, with steep slopes facing distally and shallow slopes proximally. The absence of a significant direction dependence on smooth and 1-μm high microstructured surfaces suggests the effect of interlocking is masked by the stronger influence of adhesion on friction, which acts equally in both directions. Our findings show that cockroach euplantulae generate friction using both interlocking and adhesion.     

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.     

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.     

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。     

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.     

Between a rock and a soft place: microtopography of the locomotor substrate and the morphology of the setal fields of Namibian day geckos (Gekkota: Gekkonidae: Rhoptropus)

Many species of gekkotans possess adhesive subdigital pads that allow them to adhere to, and move on, a wide variety of surfaces. The natural surfaces exploited by these lizards may be rough, undulant and unpredictable and therefore likely provide only limited, patchy areas for adhesive contact. Here, we examine the microtopography of rock surfaces used by seven species of Rhoptropus and compare this to several rough and smooth artificial surfaces employed in previous studies of gekkotan adhesion. These data are considered in relation to the form, configuration, compliance and functional morphology of the setal fields of these species. Our results demonstrate that natural rock surfaces are rough and unpredictable at the scale of the setal arrays, with equal amounts of variation existing within and between the various types of rock surfaces examined. Such surfaces differ from smooth and rough artificial surfaces in the proportion of surface area available for attachment and the relative predictability of surface undulance. Generally, setal field characteristics of individual species are not relatable to specific substrates, but instead are configured to allow for sufficient attachment to a wide variety of unpredictable surfaces. Our findings provide insight into the evolution and microanatomy of the adhesive system of gekkotan lizards and its adaptive relationship to topographically unpredictable surfaces.     

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.     

Cover Caption

Cover: The leaf beetle Gastrophysa viridula clinging to the surface of its host plant, the dock leaf (Rumex). The beetle uses both its claws and hairy adhesive pads to climb on a variety of surface profiles. Its ability to attach to rough and smooth substrates was investigated by James Bullock and Walter Federle who found that attachment performance varies as the roughness scale increase or decreases relative to the tip size of the beetle's adhesive hairs. See pages 298‐304. Photo credit: Thomas Endlein.     

Microstructure of the tarsal adhesive organs in the bark beetle Ips acuminatus,and their implication as external carriers of pathogens

Ips acuminatus is a common group of bark beetles that infest and damage pine and spruce trees. As a part of research for controlling this insect pest, the adhesive organs on the tarsal appendages were examined using field emission scanning electron microscopy (FE-SEM) to reveal the microstructural characteristics of its biological attachment system. In addition, we also demonstrate their ability to act as external carriers of pathogens. This bark beetle has a characteristic attachment apparatus to move both smooth and rough surfaces. The claws are connected with a pretarsal segment, and their apical diverged hooks are developed to hold rough substrates; however, landing on smooth surfaces is achieved by means of three groups of hairy tarsal pads. The adhesive pads are basically composed of the flattened tip setae usually with a spatula-shaped endplate. Although this bark beetle did not have mycangial cavities, yeast-like spores were concentrated at the invaginated surface of legs where cuticular hairs are densely packed. In particular, the base stalk of the adhesive pad had a sufficient space to accept spores during the dynamic movement of tenent setae.     

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。     

Pushing versus pulling: division of labour between tarsal attachment pads in cockroaches

Adhesive organs on the legs of arthropods and vertebrates are strongly direction dependent, making contact only when pulled towards the body but detaching when pushed away from it. Here we show that the two types of attachment pads found in cockroaches (Nauphoeta cinerea), tarsal euplantulae and pretarsal arolium, serve fundamentally different functions. Video recordings of vertical climbing revealed that euplantulae are almost exclusively engaged with the substrate when legs are pushing, whereas arolia make contact when pulling. Thus, upward-climbing cockroaches used front leg arolia and hind leg euplantulae, whereas hind leg arolia and front leg euplantulae were engaged during downward climbing. Single-leg friction force measurements showed that the arolium and euplantulae have an opposite direction dependence. Euplantulae achieved maximum friction when pushed distally, whereas arolium forces were maximal during proximal pulls. This direction dependence was not explained by the variation of shear stress but by different contact areas during pushing or pulling. The changes in contact area result from the arrangement of the flexible tarsal chain, tending to detach the arolium when pushing and to peel off euplantulae when in tension. Our results suggest that the euplantulae in cockroaches are not adhesive organs but 'friction pads', mainly providing the necessary traction during locomotion.     

Insect walking techniques on thin stems

The attachment ability of insects on surfaces are associated not only with the micro- and nanostructure of the adhering part of an attachment device, but also with the global scale kinematics responsible for contact formation and release. In the present study, the locomotory techniques of several representatives of insects from four different orders (Orthoptera, Heteroptera, Coleoptera, and Hymenoptera), possessing different types of attachment structures, are described. The study is based on video recordings of insects walking on a flat surface and on cylindrical rods of various thickness, imitating plant stems. Attachment devices of tarsi and pretarsi were visualized using Scanning Electron Microscopy. The results show a different manner in the use of adhesive structures on substrates with various curvatures. Insects bearing attachment pads on proximal tarsomeres usually touch flat and curved substrates using all tarsomeres, whereas insects with their attachment devices on the distal tarsomeres usually walk on flat surfaces using the distal tarsomeres of the overextended tarsus. On substrates, with diameters comparable to or larger than the tarsus length, insects walk above the stem by clasping the stem with the bent tarsi. On thin stems, insects clasp the stem between their tarsi and hang under the stem. Thus, on thin and thick rods, forces applied to attachment organs act in opposite directions. There are two methods of leg positioning for walking on a rough flat substrate. In the first case, the tarsus is straightened and the rough substrate is gripped between the claws and the proximal complex of attachment devices (tarsal euplantulae, fossulae spongiosa, and terminal spurs of tibiae). In the second case the tibia does not touch the substrate; the insect is supported only by distal tarsomeres. The tarsus is in an overextended condition. On rods, with diameters comparable to or larger than the tarsus length, insects walk by clasping the stem with the bent tarsi. This posture is characteristic for the majority of insects independent of the tarsal position they normally use while walking on a plane. If the rod’s diameter is smaller than the tarsus length, walking insects usually clutch it between contralateral tarsi. Using such a posture they are supported by interlocking or by strong friction, generated by attachment devices of the proximal tarsomeres, and do not use attachment devices of the pretarsus. Contact with the substrate is reinforced due to the coordinated contralateral clutch using all supporting legs. It is concluded that the use of different types of attachment structures correlates with locomotory techniques. Handling Editor: Heikki Hokkanen     

Changes in tarsal morphology and attachment ability to rough surfaces during ontogenesis in the beetle Gastrophysa viridula (Coleoptera,Chrysomelidae)

Insects live in a three-dimensional space, and need to be able to attach to different types of surfaces in a variety of environmental and behavioral contexts. Adult leaf beetles possess great attachment ability due to their hairy attachment pads. In contrast, their larvae depend on smooth pads to attach to the same host plant. We tested friction forces generated by larvae and adults of dock leaf beetles Gastrophysa viridula on different rough surfaces, and found that adults generate much higher attachment to various substrates than larvae, but are more susceptible to completely losing attachment ability on surfaces with “critical” roughness. Furthermore, sex-specific setal morphology has the effect that attachment forces of male adults are generally higher than those of females when adjusted for body weight. The results are discussed in the context of development, ecology, and changing behavioral strategies of successive life stages.     

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.     

How do sucker‐footed bats hold on,and why do they roost head‐up?

Individuals of most bat species hang head‐down by their toenails from rough surfaces, but Madagascar's endemic sucker‐footed bat (Myzopoda aurita) clings head‐up to smooth leaves using specialized pads on its wrists and ankles. We investigated the adhesive performance of 28 individuals and found that attachment performance on brass was not affected by the presence or absence of a seal around the pad–surface interface. Furthermore, on smooth acrylic, the wrist pads were more than nine‐fold weaker when lifted perpendicular to the surface than when pulled parallel to it. The unimportance of a seal and the difference in strength in those directions on a smooth surface are characteristic of wet adhesion, but not of suction. Thus, despite its name, the sucker‐footed bat appears to adhere using wet adhesion. We observed that when wrist pads were pushed anteriorly, they unpeeled easily from the surface because of deformation of the pads. This most likely permits rapid detachment during crawling, but would also cause passive detachment if bats roosted head‐down. This provides an ecomorphological explanation to the head‐up roosting behaviour of these unique bats. The results obtained in the present study thus link morphology, behaviour, and roosting ecology for an enigmatic Malagasy endemic. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 233–240.     

Nonlinear variation in clinging performance with surface roughness in geckos

Understanding the challenges faced by organisms moving within their environment is essential to comprehending the evolution of locomotor morphology and habitat use. Geckos have developed adhesive toe pads that enable exploitation of a wide range of microhabitats. These toe pads, and their adhesive mechanisms, have typically been studied using a range of artificial substrates, usually significantly smoother than those available in nature. Although these studies have been fundamental in understanding the mechanisms of attachment in geckos, it is unclear whether gecko attachment simply gradually declines with increased roughness as some researchers have suggested, or whether the interaction between the gekkotan adhesive system and surface roughness produces nonlinear relationships. To understand ecological challenges faced in their natural habitats, it is essential to use test surfaces that are more like surfaces used by geckos in nature. We tested gecko shear force (i.e., frictional force) generation as a measure of clinging performance on three artificial substrates. We selected substrates that exhibit microtopographies with peak‐to‐valley heights similar to those of substrates used in nature, to investigate performance on a range of smooth surfaces (glass), and fine‐grained (fine sandpaper) to rough (coarse sandpaper). We found that shear force did not decline monotonically with roughness, but varied nonlinearly among substrates. Clinging performance was greater on glass and coarse sandpaper than on fine sandpaper, and clinging performance was not significantly different between glass and coarse sandpaper. Our results demonstrate that performance on different substrates varies, probably depending on the underlying mechanisms of the adhesive apparatus in geckos.     

Ground reaction forces in vertically ascending beetles and corresponding activity of the claw retractor muscle on smooth and rough substrates

We measured ground reaction forces in fore–aft and normal directions of single hind and front legs in vertically ascending Sagra femorata beetles (Coleoptera, Chrysomelidae) on a smooth and a rough substrate. Simultaneously, we performed electromyographic recordings (EMGs) of the hind leg claw retractor muscle that partly controls the attachment structures. On both substrates, hind legs produced upward- as well as downward-directed forces during one stance phase. Forces were equivalent in both directions. Front legs generated only upward-directed forces. The main function of hind legs in ascending beetles in the second half of the stance thus probably prevented the animals from tilting away from the substrate. The EMGs of hind legs showed an early spike during stance with large amplitude. It was mostly followed by few additional spikes with large amplitude and in some cases of spikes with smaller amplitude distributed throughout the stance phase. We found significantly more spikes on the rough substrate than on the smooth one. This is probably due to the more important role of pretarsal claws than tarsal hairy attachment pads on the rough substrate or to the reduced adhesive forces on the rough substrate that have to be compensated by additional muscle activity.     

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.