Adhesive Toe Pads Research Articles

Self-drying: a gecko's innate ability to remove water from wet toe pads.

When the adhesive toe pads of geckos become wet, they become ineffective in enabling geckos to stick to substrates. This result is puzzling given that many species of gecko are endemic to tropical environments where water covered surfaces are ubiquitous. We hypothesized that geckos can recover adhesive capabilities following exposure of their toe pads to water by walking on a dry surface, similar to the active self-cleaning of dirt particles. We measured the time it took to recover maximum shear adhesion after toe pads had become wet in two groups, those that were allowed to actively walk and those that were not. Keeping in mind the importance of substrate wettability to adhesion on wet surfaces, we also tested geckos on hydrophilic glass and an intermediately wetting substrate (polymethylmethacrylate; PMMA). We found that time to maximum shear adhesion recovery did not differ in the walking groups based on substrate wettability (22.7±5.1 min on glass and 15.4±0.3 min on PMMA) but did have a significant effect in the non-walking groups (54.3±3.9 min on glass and 27.8±2.5 min on PMMA). Overall, we found that by actively walking, geckos were able to self-dry their wet toe pads and regain maximum shear adhesion significantly faster than those that did not walk. Our results highlight a unexpected property of the gecko adhesive system, the ability to actively self-dry and recover adhesive performance after being rendered dysfunctional by water.

Stick or grip? Co-evolution of adhesive toepads and claws in Anolis lizards

Exploring the relationship between phenotype and performance in an ecological and evolutionary context is crucial to understanding the adaptive nature of phenotypic traits. Despite their ubiquity in vertebrates, few studies have examined the functional and ecological significance of claw morphologies. Here we examine the adhesive toepad and claw system of Anolis lizards. Claw characters are significantly different between lizards classified as arboreal (perch height≥1m) and non-arboreal (perch height<1m). Arboreal species possess significantly higher and longer claws, and show trends toward decreased claw curvature and wider claw tip angles. Toepad size and claw length and height are tightly correlated with each other and with perch height, suggesting that the adhesive toepad and gripping claw have co-evolved to accommodate different habitats. The functional morphology and evolution of claws are ripe areas for future investigation.

Key innovations and island colonization as engines of evolutionary diversification: a comparative test with theAustralasian diplodactyloid geckos

The acquisition of key innovations and the invasion of new areas constitute two major processes that facilitate ecological opportunity and subsequent evolutionary diversification. Using a major lizard radiation as a model, the Australasian diplodactyloid geckos, we explored the effects of two key innovations (adhesive toepads and a snake-like phenotype) and the invasion of new environments (island colonization) in promoting the evolution of phenotypic and species diversity. We found no evidence that toepads had significantly increased evolutionary diversification, which challenges the common assumption that the evolution of toepads has been responsible for the extensive radiation of geckos. In contrast, a snakelike phenotype was associated with increased rates of body size evolution and, to a lesser extent, species diversification. However, the clearest impact on evolutionary diversification has been the colonization of New Zealand and New Caledonia, which were associated with increased rates of both body size evolution and species diversification. This highlights that colonizing new environments can drive adaptive diversification in conjunction or independently of the evolution of a key innovation. Studies wishing to confirm the putative link between a key innovation and subsequent evolutionary diversification must therefore show that it has been the acquisition of an innovation specifically, not the colonization of new areas more generally, that has prompted diversification.

Comparative Cryo-SEM and AFM studies of hylid and rhacophorid tree frog toe pads

Cryo-scanning electron microscopy (cryo-SEM) and atomic force microscopy (AFM) offer new avenues for the study of the morphology of tree frog adhesive toe pads. Using these techniques, we compare toe pad microstructure in two distantly related species of tree frog, Litoria caerulea, White (Hylidae) and Rhacophorus prominanus, Smith (Rhacophoridae), in which the toe pads are considered to be convergent. AFM demonstrates the extraordinary similarity of both surface microstructures (largely hexagonal epithelial cells surrounded by deep channels) and nanostructures (an array of nanopillars, ca. 350 nm in diameter, all with a small dimple at the apex). The cryo-SEM studies examined the distribution of the fibrillar cytoskeleton within the different layers of the stratified toe pad epithelium, demonstrating that the cytoskeletal elements (keratin tonofilaments) that lie at an angle to the surface are relatively poorly developed in L. caerulea, clearly so in comparison to R. prominanus. Cryo-SEM also enabled the visualization of the fluid layer that is critical to a toe pad's adhesive function. This was achieved by examination of the frozen fluid residues left behind after removal of a toe within the cryo-SEM's experimental chamber. Such 'toeprints' demonstrated the presence of a wedge of fluid surrounding each toe pad, as well as fluid filling the channels that surround each epithelial cell. Cryo-SEM was used to examine epithelial cell shape. In a sample of 582 cells, 59.5% were hexagonal, the remainder being mainly pentagonal (23.1%) or heptagonal (16.1%). The distribution of differently-shaped cells was not random, but was not associated with either pad curvature or the distribution of mucous pores that provide fluid for the frogs' wet adhesion mechanism. Our main finding, the great similarity of toe pad structure in these two species, has important implications for biomimetics, for such convergent evolution suggests a good starting point for attempts to develop adhesives that will function in wet conditions.

Self-cleaning in tree frog toe pads; a mechanism for recovering from contamination without the need for grooming

Tree frogs use adhesive toe pads for climbing on a variety of surfaces. They rely on wet adhesion, which is aided by the secretion of mucus. In nature, the pads will undoubtedly get contaminated regularly through usage, but appear to maintain their stickiness over time. Here, we show in two experiments that the toe pads of White's tree frogs (Litoria caerulea) quickly recover from contamination through a self-cleaning mechanism. We compared adhesive forces prior to and after contamination of (1) the whole animal on a rotatable platform and (2) individual toe pads in restrained frogs mimicking individual steps using a motorised stage. In both cases, the adhesive forces recovered after a few steps but this took significantly longer in single toe pad experiments from restrained frogs, showing that use of the pads increases recovery. We propose that both shear movements and a 'flushing' effect of the secreted mucus play an important role in shedding particles/contaminants.

The effect of surface water and wetting on gecko adhesion

Despite profound interest in the mechanics and performance of the gecko adhesive system, relatively few studies have focused on performance under conditions that are ecologically relevant to the natural habitats of geckos. Because geckos are likely to encounter surfaces that are wet, we used shear force adhesion measurements to examine the effect of surface water and toe pad wetting on the whole-animal performance of a tropical-dwelling gecko (Gekko gecko). To test the effect of surface wetting, we measured the shear adhesive force of geckos on three substrate conditions: dry glass, glass misted with water droplets and glass fully submerged in water. We also investigated the effect of wetting on the adhesive toe pad by soaking the toe pads prior to testing. Finally, we tested for repeatability of the adhesive system in each wetting condition by measuring shear adhesion after each step a gecko made under treatment conditions. Wetted toe pads had significantly lower shear adhesive force in all treatments (0.86 ± 0.09 N) than the control (17.96 ± 3.42 N), as did full immersion in water (0.44 ± 0.03 N). Treatments with droplets of water distributed across the surface were more variable and did not differ from treatments where the surface was dry (4.72 ± 1.59 N misted glass; 9.76 ± 2.81 N dry glass), except after the gecko took multiple steps. These findings suggest that surface water and the wetting of a gecko's adhesive toe pads may have significant consequences for the ecology and behavior of geckos living in tropical environments.

Repeated origin and loss of adhesive toepads in geckos.

Geckos are well known for their extraordinary clinging abilities and many species easily scale vertical or even inverted surfaces. This ability is enabled by a complex digital adhesive mechanism (adhesive toepads) that employs van der Waals based adhesion, augmented by frictional forces. Numerous morphological traits and behaviors have evolved to facilitate deployment of the adhesive mechanism, maximize adhesive force and enable release from the substrate. The complex digital morphologies that result allow geckos to interact with their environment in a novel fashion quite differently from most other lizards. Details of toepad morphology suggest multiple gains and losses of the adhesive mechanism, but lack of a comprehensive phylogeny has hindered efforts to determine how frequently adhesive toepads have been gained and lost. Here we present a multigene phylogeny of geckos, including 107 of 118 recognized genera, and determine that adhesive toepads have been gained and lost multiple times, and remarkably, with approximately equal frequency. The most likely hypothesis suggests that adhesive toepads evolved 11 times and were lost nine times. The overall external morphology of the toepad is strikingly similar in many lineages in which it is independently derived, but lineage-specific differences are evident, particularly regarding internal anatomy, with unique morphological patterns defining each independent derivation.

Elastic modulus of tree frog adhesive toe pads

Previous work using an atomic force microscope in nanoindenter mode indicated that the outer, 10- to 15-μm thick, keratinised layer of tree frog toe pads has a modulus of elasticity equivalent to silicone rubber (5–15 MPa) (Scholz et al. 2009), but gave no information on the physical properties of deeper structures. In this study, micro-indentation is used to measure the stiffness of whole toe pads of the tree frog, Litoria caerulea. We show here that tree frog toe pads are amongst the softest of biological structures (effective elastic modulus 4–25 kPa), and that they exhibit a gradient of stiffness, being stiffest on the outside. This stiffness gradient results from the presence of a dense network of capillaries lying beneath the pad epidermis, which probably has a shock absorbing function. Additionally, we compare the physical properties (elastic modulus, work of adhesion, pull-off force) of the toe pads of immature and adult frogs.Electronic supplementary materialThe online version of this article (doi:10.1007/s00359-011-0658-1) contains supplementary material, which is available to authorized users.

Histochemical and ultrastructural analyses of adhesive setae of lizards indicate that they contain lipids in addition to keratins

We studied the distribution of lipid material and organelles in the epidermal layers of toe pads from two species of lizards representing the two main lizard families in which adhesive scansors are found (gekkonids and polychrotids), the dull day gecko, Phelsuma dubia and the green anole, Anolis carolinensis. Although lipids are a conspicuous component of the mesos layer of squamate reptiles and function in reducing cutaneous water loss, their distribution has not been specifically studied in the highly elaborated epidermal surface of adhesive toe pads. We found that, in addition to the typical cutaneous water loss-resistant mesos and alpha-layer lipids, the Oberhutchen (including the setae) on the most exterior layers of the epidermis in P. dubia and A. carolinensis also contain lipid material. We also present detailed histochemical and ultrastructural analyses of the toe pads of P. dubia, which indicate that lipid material is closely associated spatially with maturing setae as they branch during the renewal phase of epidermal regeneration. This lipid material appears associated with the packing of keratin within setae, possibly affecting permeability to water loss in the pad lamella, where the surface area is from 4–60-fold greater compared with normal scales.

A 100 million year old gecko with sophisticated adhesive toe pads, preserved in amber from Myanmar

A 100 million year old gecko with sophisticated adhesive toe pads, preserved in amber from Myanmar

A 100 million year old gecko with sophisticated adhesive toe pads, preserved in amber from Myanmar

A new genus and species of gecko is described from a posterior lower limb and foot, and a partial tail, preserved in Lower Cretaceous amber from Myanmar that is 97–110My old. It appears to be the oldest unequivocal fossil gecko, predating fragmentary skeletal remains from the Upper Cretaceous and being 43–56 My older than Yanatarogecko from the Lower Eocene, previously the oldest known gecko preserved in amber. It also provides firm evidence that gekkotans and possibly gekkonids were in Asia at this time. The Myanmar specimen shows, that the distinctive foot proportions and sophisticated adhesive mechanism, involving pads on the toes with transverse lamellae probably bearing numerous hairlike setae found in many modern geckos, had already evolved around 100My ago. The specimen is very small, even compared with juveniles of the smallest living geckos. However, the high numbers of lamellae on its toe pads suggest it is from a juvenile of a species with relatively large adult body size.

Wet adhesion with application to tree frog adhesive toe pads and tires

Strong adhesion between solids with rough surfaces is only possible if at least one of thesolids is elastically very soft. Some lizards and spiders are able to adhere (dryadhesion) and move on very rough vertical surfaces due to very compliant surfacelayers on their attachment pads. Flies, bugs, grasshoppers and tree frogs have lesscompliant pad surface layers, and in these cases adhesion to rough surfaces isonly possible because the animals inject a wetting liquid into the pad–substratecontact area, which generates a relative long-range attractive interaction due to theformation of capillary bridges. In this presentation I will discuss some aspects ofwet adhesion for tree frogs and give some comments related to tire applications.

Editorial

Editorial

Wet but not slippery: boundary friction in tree frog adhesive toe pads

Tree frogs are remarkable for their capacity to cling to smooth surfaces using large toe pads. The adhesive skin of tree frog toe pads is characterized by peg-studded hexagonal cells separated by deep channels into which mucus glands open. The pads are completely wetted with watery mucus, which led previous authors to suggest that attachment is solely due to capillary and viscous forces generated by the fluid-filled joint between the pad and the substrate. Here, we present evidence from single-toe force measurements, laser tweezer microrheometry of pad mucus and interference reflection microscopy of the contact zone in Litoria caerulea, that tree frog attachment forces are significantly enhanced by close contacts and boundary friction between the pad epidermis and the substrate, facilitated by the highly regular pad microstructure.

Dynamics of geckos running vertically

Geckos with adhesive toe pads rapidly climb even smooth vertical surfaces. We challenged geckos (Hemidactylus garnotii) to climb up a smooth vertical track that contained a force platform. Geckos climbed vertically at up to 77 cm s(-1) with a stride frequency of 15 Hz using a trotting gait. During each step, whole body fore-aft, lateral and normal forces all decreased to zero when the animal attached or detached its toe pads. Peak fore-aft force was twice body weight at mid-step. Geckos climbed at a constant average velocity without generating decelerating forces on their center of mass in the direction of motion. Although mass-specific mechanical power to climb was ten times the value expected for level running, the total mechanical energy of climbing was only 5-11% greater than the potential energy change. Fore- and hindlegs both pulled toward the midline, possibly loading the attachment mechanisms. Attachment and detachment of feet occupied 13% and 37% of stance time, respectively. As climbing speed increased, the absolute time required to attach and detach did not decrease, suggesting that the period of fore-aft force production might be constrained. During ascent, the forelegs pulled toward, while hindlegs pushed away from the vertical surface, generating a net pitching moment toward the surface to counterbalance pitch-back away from the surface. Differential leg function appears essential for effective vertical as well as horizontal locomotion.

Morphology and morphometrics of the appendicular musculature in geckoes with different locomotor habits (Lepidosauria)

In this study a ground-dwelling (Eublepharis macularius) and a highly specialised climbing (Gekko gecko) lizard were chosen as study objects. The fore- and hindlimbs of two individuals of each species were dissected, and muscle masses, mean fibre lengths, cross-sectional areas and moment arms were determined. Special attention was paid to general muscle architecture (origin, insertion, fibre orientation, etc.) and pennation angles. Using these variables (cross sectional areas and moment arms), maximal moments exertable across the shoulder/hip, elbow/knee and wrist/ankle were calculated for both species. In accordance with the biomechanical predictions related to the preferred locomotor substrate of each species (i.e. level running for E. macularius and climbing for G. gecko), the results of this study indicate that climbers such as G. gecko generally possess powerful retractor muscles crossing the shoulder and hip joints. Additionally, the specialised climber is able to exert higher flexion moments across the elbow, which prevents the animals from falling backwards. However, G. gecko appears to be constrained in its ankle extension capabilities by the presence of the adhesive toe pads. The level-running species, on the other hand, shows a relatively stronger development of the extensor muscles in the lower limbs, allowing these lizards to run in an erect posture. In general, both species show large similarities on a gross morphological level as expected when considering their phylogenetic relatedness. Adaptations to their preferred locomotor substrate only become apparent when considering the functional properties (i.e. joint moments) of the appendicular musculature.

The adhesion of treefrog toe-pads to glass: cryogenic examination of a capillary adhesion system

Treefrog adhesive toe-pads in contact with a glass surface were examined with scanning electron microscopy after preparation of the specimens using cryogenic methods. Frozen two-pads lost all adhesive abilities, which may be ascribed to the freezing and cold contraction of the intermediary fluid found between the toe-pad and the substrate. Residue from this fluid remained behind on both toe-pad and the substrate. Impressions of toe-pad epithelial cells in the residue indicate that the individual cells may be relatively free to find their own closest contact with the substrate. The results corroborate earlier models indicating the importance of the intermediary fluid in a capillary adhesion system.

Digital Microstructure in Ecologically Diverse Sympatric Microhylid Frogs, Genera Cophixalus and Sphenophryne (Amphibia, Anura), From Papua-New-Guinea

The extent of development of digital adhesive toe-pads in sympatric species of microhylid frogs, Cophixalus and Sphenophryne, correlates with the degree of arboreality exhibited by the species. The same basic structures and cell types are found in the toe-pads of these microhylid frogs as are found in other arboreal and semi- arboreal frogs of many diverse evolutionary lineages. A variety of types of cell surface, with unknown functional significance but potential systematic use, are found on the feet of these frogs. Allometric increase in adhesive-pad area in larger species is by widening of the toe-pad, as opposed to acquisition of accessory pads as in some hylid tree frogs.

Reproductive Effort in Anoline Lizards

Lizards in the large neotropical genus Anolis exhibit an unusual mode of reproduction; all species lay a clutch of a single egg. In contrast, the more typical pattern for lizards is a multi—egg clutch in which the number of eggs increases with female size both inter— and intra—specifically. In Anolis low clutch number is associated with a potential for frequent ovipositions. Field rates for several tropical forest species are one egg every 1—2 wk. Thus, high rates of egg production coupled with a generation time of about 4 mo gives these species very high reproductive potentials. The evolution of low clutch number in relatively small tropical lizards has several non—exclusive explanations. One, which is specific to arboreal lizards (Anolis, geckonids, and some scincids), involves their adhesive toe pads, which facilitate climbing. Because pad area increases by the square of linear dimensions while body weight increases by the cube, pad area may put a limit both on lizard size and the weight of reproductive materials carried at any one time. A second and more general explanation involves the association between clutch size and climatic regime. Lizards in temperate and seasonal tropical habitats have a larger clutch number than do lizards of relatively equable tropical habitats. In these latter habitats short—term fluctuations in rainfall (associated with reproductive success) favor genotypes that are opportunistic reproducers, and relatively high predation intensity favors r—selected life history patterns. Anoline lizards are “extreme” examples of species living under such selective regimes.