Walking on smooth or rough ground: passive control of pretarsal attachment in ants

The hymenopteran tarsus is equipped with claws and a movable adhesive pad (arolium). Even though both organs are specialised for substrates of different roughness, they are moved by the same muscle, the claw flexor. Here we show that despite this seemingly unfavourable design, the use of arolium and claws can be adjusted according to surface roughness by mechanical control. Tendon pull experiments in ants (Oecophylla smaragdina) revealed that the claw flexor elicits rotary movements around several (pre-) tarsal joints. However, maximum angular change of claws, arolium and fifth tarsomere occurred at different pulling amplitudes, with arolium extension always being the last movement. This effect indicates that arolium use is regulated non-neuronally. Arolium unfolding can be suppressed on rough surfaces, when claw tips interlock and inhibit further contraction of the claw flexor or prevent legs from sliding towards the body. To test whether this hypothesised passive control operates in walking ants, we manipulated ants by clipping claw tips. Consistent with the proposed control mechanism, claw pruning resulted in stronger arolium extension on rough but not on smooth substrates. The control of attachment by the insect claw flexor system demonstrates how mechanical systems in the body periphery can simplify centralised, neuro-muscular feedback control.     

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。     

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.     

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。     

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.     

Locomotion and adhesion: dynamic control of adhesive surface contact in ants

Tarsal adhesive pads of insects are highly dynamic organs that play an important role in locomotion. Many insects combine fast running performance with strong resistance to detachment forces. This capacity requires an effective control of attachment forces at the tarsus and pretarsus. Here we investigate mechanisms of attachment control in Asian weaver ants (Oecophylla smaragdina) by measuring the dynamics of the adhesive contact area and the claws during locomotion. O. smaragdina ants walking upside down on a smooth substrate used only a fraction (approx. 14%) of their maximum possible contact area. When these ants were loaded with 30 mg weights (corresponding to approx. 6 times their own body weight), however, they employed much larger (but still submaximal; approx. 60%) contact areas. The increase of contact area was accompanied by a stronger flexion of the claws, which demonstrates the participation of the claw flexor muscle in the control of adhesive contact. However, only part of the contact area dynamics could be explained by the action of the claw flexor. During the stance phase, adhesive contact area changed while the claws remained motionless. Even when corrected for the effects of claw flexion, adhesive contact areas differed by a factor of 2.1 between loaded and unloaded ants. Our findings give evidence that running ants control their adhesive contact area by a combination of active movements of the claw flexor muscle and passive reactions of the mechanical system.     

Relationships among morphology, clinging performance and habitat use in Liolaemini lizards

The central tenet of ecomorphological theory holds that different ecological requirements lead to different organismal designs (morphology). Here, we studied the relationships between performance (interlocking grasping) and forelimb morphological traits in species of lizards that exploit different structural habitats in a phylogenetic context. The performance (measured by the maximum force of clinging to substrate) was measured on different substrate types. After phylogenetically informed analyses, we found that arboreal and saxicolous species showed stronger resistance to mechanical traction in all substrates when compared to generalists and sand dweller lizards. These species showed a positive relationship between forelimb dimensions (humerus length and length of claw of toe 5) and maximum force exerted, on the contrary, hand width, claw height (CH) of digits III and IV and claw length of toe 4 showed a negative relationship. In addition, we observed a partial positive correlation between CH and maximal cling force on rough surfaces, but not on smooth surfaces.     

Structure and mechanics of the tarsal chain in the hornet, Vespa crabro (Hymenoptera: Vespidae): implications on the attachment mechanism

Two combined mechanisms on the hornet tarsus are adapted to attachment to the substrate: a friction-based (claws and spines) and an adhesion-based one (arolium). There are two ranges of substrate roughness optimal for attachment, either very smooth or very rough. There is an intermediate range of substrate grains of small but non-zero size, where both of these mechanisms fail. The optimal size of substrate grains for hornet grasping was 50-100 microm. Maximal hold to the substrate was achieved when surface irregularities were clamped between the claws of opposite legs. In such a position, the insect could withstand an external force which was almost 25 times larger than its own weight. The tarsal chain is an important part of the entire attachment mechanism. The articulations in the kinematic chain of tibia-tarsus-pretarsus are monocondylar. Three tarsal muscles and one head of the claw retractor muscle originate in the tibia. On pull to the retractor tendon, the tarsus bends in a plane. All elements of the tarsal kinematic chain have one active degree of freedom. The distance between the intertarsomeric articulation point and the tendon of the claw retractor (75-194 microm) corresponds to an efficiency of 1 degrees per 1-3 mircom of pulling distance travelled by the tendon. The claw turns about 1 degrees per 4.3-5.0 microm of pulling distance travelled by the unguitractor. The arolium turns forward and downward simultaneously with flexion of the claws. The kinematic chain of the arolium lacks real condylar joints except the joint at the base of the manubrium. Other components are tied by flexible transmissions of the membranous cuticle. The walking hornet rests on distal tarsomeres of extended tarsi. If the retractor tendon inside the tarsus is fixed, passive extension of the tarsomeres might be replaced by claw flexion. Tarsal chain rigidity, measured with the force tester, increased when the retractor tendon was tightened. Probably, pull to the tendon compresses the tarsomeres, increasing friction within contacting areas of rippled surfaces surrounding condyles within articulations.     

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.     

Righting kinematics in beetles (Insecta: Coleoptera)

Twenty modes of stereotyped righting motions were observed in 116 representative species of coleoptera. Methods included cine and stereocine recording with further frame by frame analysis, stereogrammetry, inverse kinematic reconstruction of joint angles, stroboscopic photography, recording of electromyograms, 3D measurements of the articulations, etc. The basic mode consists of a search phase, ending up with grasping the substrate, and a righting, overturning phase. Leg coordination within the search cycle differs from the walking cycle with respect to phasing of certain muscle groups. Search movements of all legs appear chaotic, but the tendency to move in antiphase is still present in adjacent ipsilateral and contralateral leg pairs. The system of leg coordination might be split: legs of one side might search, while contralateral legs walk, or fore and middle legs walk while hind legs search. Elaborated types of righting include somersaults with the aid of contralateral or diagonal legs, pitch on elytra, jumps with previous energy storage with the aid of unbending between thoracic segments (well-known for Elateridae), or quick folding of elytra (originally described in Histeridae). Righting in beetles is compared with righting modes known in locusts and cockroaches. Search in a righting beetle is directed dorsad, while a walking insect searches for the ground downwards. Main righting modes were schematized for possible application to robotics.     

Comparative morphology of pretarsal scopulae in eleven spider families

Many wandering spiders bear attachment pads (scopulae) on their tarsi, consisting of hierarchically-branching adhesive setae. Amongst spider families and even species, these show remarkable differences in morphology. Using scanning electron microscopy, the scopula microstructure of sixteen spider species was described, with the focus on pretarsal scopulae (claw tufts). Area and shape of the claw tuft, seta and setule density, as well as seta and spatula dimensions were analysed and compared. Claw tufts of the majority of species studied show a similar gradient in size and shape from anterior to posterior legs: the dimension of pads increases, while setal density decreases. Commonly, there is also a gradient of both the seta and spatula size within the claw tuft: Setae become larger from the proximal to the distal part of the pad, and spatulae size increases in the same direction at the level of individual seta. Often, different hierarchical levels of claw tuft organisation are differently expressed in different species: Species with lower setal density usually have broader setae. Smaller spatula size often implicates higher setule density. Evolutionary and ecological aspects of the scopula origin are discussed.     

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.     

The effect of surface roughness on claw and adhesive hair performance in the dock beetle Gastrophysa viridula

Abstract Natural adhesive systems are adapted to attach to rough surfaces, but the underlying mechanisms have not been fully clarified. Attachment forces for the beetle Gastrophysa viridula were recorded on epoxy casts of surfaces with different roughness using a centrifuge device. Replicas were made of standardized polishing paper with asperity sizes ranging from 0.05 to 30 μm and of dock leaves (Rumex obtusifolius). Beetles adhered with a safety factor of up to 36 times body weight on smooth substrates or on casts of leaves of their host plant. On the rough substrates, forces were much lower and a minimum at small scale roughness (0.05 μm asperity size, with a mean safety factor of 5) was observed. Removal of the claws led to a significant reduction in force for rough substrates with asperity sizes ≥ 12 μm. Attachment forces of the hairy adhesive system itself (without the claws) slightly increased from small‐scale to large‐scale surface roughness, but remained below the level seen on the smooth substrate. This is explained by the inability of setal tips to make full contact to the surface.     

Surface Response of Fluorine Polymer-Incorporated Resin Composites to Cariogenic Biofilm Adherence

Experimental resin composites with incorporated polytetrafluoroethylene (PTFE) particles were developed, which theoretically could improve the surface properties of the materials, including the inhibition of bacterial adherence. To assess the surface properties in relation to biofilm formation and detachment, 23.1% (wt/wt) linear PTFE particles (FL-30) and cross-linked PTFE particles (FC-30) were incorporated into pure resin composites. Pure PTFE plates and pure resin composites without PTFE (F-0) were used as control specimens. Sucrose-dependent Streptococcus mutans biofilms were formed on the specimen blocks inside an oral biofilm reactor for various time periods and analyzed with or without application of driving forces. In addition, water contact angles and surface roughness were measured. The water contact angles of FL-30 (61.2°) and FC-30 (65.8°) were larger than that of F-0 (48.5°). The largest contact angle (107°) was detected on pure PTFE plates. However, the surfaces of FL-30, FC-30, and pure PTFE plates were rougher than that of F-0. Although the surface properties of the materials differed in terms of contact angles and roughness, these factors seemed not to affect biofilm formation on the surfaces within 5 h. Pure PTFE plates harbored almost the same amounts of biofilm as F-0. However, when a very strong driving force was applied, it was clear that there were significantly smaller amounts of biofilms retained on pure PTFE plates, which showed contact angles much higher than those of the other materials. Hydrophobicity of the resin composite was improved by incorporation of PTFE fillers. However, surface resistance against biofilm formation was not improved.     

Position-dependent sensitivity and density of taste receptors on the locust leg underlies behavioural effectiveness of chemosensory stimulation

Chemical stimulation of contact chemoreceptors located on the legs of locusts evokes withdrawal movements of the leg. The likelihood of withdrawal depends on the site of stimulation, in addition to the identity and concentration of the chemical stimulus. A significantly higher percentage of locusts exhibit leg avoidance movements in response to stimulation of distal parts of the leg with any given chemical stimulus compared to proximal sites. Moreover, the percentage of locusts exhibiting avoidance movements is correlated with the density and sensitivity of chemoreceptors on different sites of an individual leg. The effectiveness of chemical stimulation also differs between the fore and hind legs, with NaCl evoking a higher probability of leg withdrawal movements on the foreleg. Moreover, sucrose was less effective than NaCl at evoking withdrawal movements of the foreleg, particularly at low concentrations. The gradients in behavioural responses can be partially attributed to differences in the responsiveness and density of the contact chemoreceptors. These results may reflect the different specialization of individual legs, with the forelegs particularly involved in food selection.     

Friction and adhesion in the tarsal and metatarsal scopulae of spiders

Friction and adhesion forces of the ventral surface of tarsi and metatarsi were measured in the bird spider Aphonopelma seemanni (Theraphosidae) and the hunting spider Cupiennius salei (Ctenidae). Adhesion measurements revealed no detectable attractive forces when the ventral surfaces of the leg segments were loaded and unloaded against the flat smooth glass surface. Strong friction anisotropy was observed: friction was considerably higher during sliding in the distal direction. Such anisotropy is explained by an anisotropic arrangement of microtrichia on setae: only the setal surface facing in the distal direction of the leg is covered by the microtrichia with spatula-like tips. When the leg is pushed, the spatula-shaped tips of microtrichia contact the substrate, whereas, when the leg is pulled over a surface, setae bend in the opposite direction and contact the substrate with their spatulae-lacking sides. In an additional series of experiments, it was shown that desiccation has an effect on the friction force. Presumably, drying of the legs results in reduction of the flexibility of the setae, microtrichia, spatulae, and underlying cuticle; this diminishes the ability to establish proper contact with the substrate and thus reduces the contact forces.     

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.     

Effect of knee joint flexion and femur rotation on retropatellar contact of the human knee joint]

The aim of the present study was to evaluate retropatellar contact characteristics at different angles of flexion of the knee joint. To this end, 6 cadaveric legs were examined using pressure sensitive film (Fuji Prescale type "super low") at angles of flexion of 45 degrees, 60 degrees, 90 degrees and 120 degrees both in neutral rotation and 10 degrees internal and external rotation of the femur in the same knee joints. A force of 140 N was applied to both the vastus medialis and lateralis, and a comparison made with a medially and a laterally dominating muscle force. The contact areas decreased with increasing angles of flexion. The medially dominating muscle traction increased the contact area. Comparison between internal and external rotation revealed a decrease in contact area on internal rotation. The pressure measurements were comparable in all loading situations. Comparison between neutral and medial traction revealed significant differences in contact area, pressure and force. The influence of femoral rotation showed no significant difference. A comparison of the different angles of flexion revealed only few significant differences. To prevent the development of retropatellar arthrosis, maximum contact areas are necessary. The study has shown an advantage for medially dominating muscle traction, and external rotation of the femur.     

The effect of vastus medialis forces on patello-femoral contact: a model-based study

A mathematical model of the patello-femoral joint was introduced to investigate the impact of the vastus medialis (longus, obliquus) forces on the lateral contact force levels. In the model, the quadriceps were represented as five separate forces: vastus lateralis, vastus intermedius, rectus femoris, vastus medialis longus (VML), and obliquus (VMO). By varying the relative force generation ratios of the quadriceps heads, the patello-femoral contact forces were estimated. We sought to analytically determine the range of forces in the VMO and VML that cause a reduction or an increase of lateral contact forces, often the cause of patello-femoral pain. Our results indicated that increased contact forces are more dependent on combinations of muscle forces than solely VMO weakness. Moreover, our simulation data showed that the contact force levels are also highly dependent on the knee flexion angle. These findings suggest that training targeted to reduce contact forces through certain joint angles could actually result in a significant increase of the contact forces through other joint angles.     

Contact behaviour of setal tips in the hairy attachment system of the fly Calliphora vicina (Diptera, Calliphoridae): a cryo-SEM approach

The fly Calliphora vicina (Diptera, Calliphoridae) bears attachment pads (pulvilli) covered with setae on their ventral sides. These structures enable attachment to smooth vertical surfaces and ceilings. The contact between the terminal setal tips (spatulae) and various substrates was visualised using various experimental techniques combined with conventional scanning electron microscopy (SEM) and cryo-SEM. The results show that the setal endplates are highly flexible structures that form contact with the surface by bending their tips in the distal direction. With conventional SEM, a comparison of partly attached endplates with unattached endplates demonstrated the presence of a distinct marginal bulge. As observed with cryo-SEM, the bulge continuously disappeared as a larger area of the endplate came into contact. Two explanations of this result are suggested. First, the volume between the bulge, the mid-part of the endplate and the substrate may be filled with a fluid secretion that is released into the contact area in the endplate region. Second, the flexible central part of the endplate may jump into contact with the substrate during contact formation.