Modeling observed animal performance using the Weibull distribution.

To understand how organisms adapt, researchers must link performance and microhabitat. However, measuring performance, especially maximum performance, can sometimes be difficult. Here, we describe an improvement over previous techniques that only consider the largest observed values as maxima. Instead, we model expected performance observations via the Weibull distribution, a statistical approach that reduces the impact of rare observations. After calculating group-level weighted averages and variances by treating individuals separately to reduce pseudoreplication, our approach resulted in high statistical power despite small sample sizes. We fitted lizard adhesive performance and bite force data to the Weibull distribution and found that it closely estimated maximum performance in both cases, illustrating the generality of our approach. Using the Weibull distribution to estimate observed performance greatly improves upon previous techniques by facilitating power analyses and error estimations around robustly estimated maximum values.

Experimental evidence for friction-enhancing integumentary modifications of chameleons and associated functional and evolutionary implications.

The striking morphological convergence of hair-like integumentary derivatives of lizards and arthropods (spiders and insects) demonstrates the importance of such features for enhancing purchase on the locomotor substrate. These pilose structures are responsible for the unique tractive abilities of these groups of animals, enabling them to move with seeming ease on overhanging and inverted surfaces, and to traverse inclined smooth substrates. Three groups of lizards are well known for bearing adhesion-promoting setae on their digits: geckos, anoles and skinks. Similar features are also found on the ventral subdigital and distal caudal skin of chameleons. These have only recently been described in any detail, and structurally and functionally are much less well understood than are the setae of geckos and anoles. The seta-like structures of chameleons are not branched (a characteristic of many geckos), nor do they terminate in spatulate tips (which is characteristic of geckos, anoles and skinks). They are densely packed and have attenuated blunt, globose tips or broad, blade-like shafts that are flattened for much of their length. Using a force transducer, we tested the hypothesis that these structures enhance friction and demonstrate that the pilose skin has a greater frictional coefficient than does the smooth skin of these animals. Our results are consistent with friction being generated as a result of side contact of the integumentary filaments. We discuss the evolutionary and functional implications of these seta-like structures in comparison with those typical of other lizard groups and with the properties of seta-mimicking synthetic structures.

Design and fabrication of gecko-inspired adhesives.

Recently, there has been significant interest in developing dry adhesives mimicking the gecko adhesive system, which offers several advantages compared to conventional pressure-sensitive adhesives. Specifically, gecko adhesive pads have anisotropic adhesion properties; the adhesive pads (spatulae) stick strongly when sheared in one direction but are non-adherent when sheared in the opposite direction. This anisotropy property is attributed to the complex topography of the array of fine tilted and curved columnar structures (setae) that bear the spatulae. In this study, we present an easy, scalable method, relying on conventional and unconventional techniques, to incorporate tilt in the fabrication of synthetic polymer-based dry adhesives mimicking the gecko adhesive system, which provides anisotropic adhesion properties. We measured the anisotropic adhesion and friction properties of samples with various tilt angles to test the validity of a nanoscale tape-peeling model of spatular function. Consistent with the peel zone model, samples with lower tilt angles yielded larger adhesion forces. The tribological properties of the synthetic arrays were highly anisotropic, reminiscent of the frictional adhesion behavior of gecko setal arrays. When a 60° tilt sample was actuated in the gripping direction, a static adhesion strength of ~1.4 N/cm(2) and a static friction strength of ~5.4 N/cm(2) were obtained. In contrast, when the dry adhesive was actuated in the releasing direction, we measured an initial repulsive normal force and negligible friction.

Changes in materials properties explain the effects of humidity on gecko adhesion.

Geckos owe their remarkable stickiness to millions of dry setae on their toes, and the mechanism of adhesion in gecko setae has been the topic of scientific scrutiny for over two centuries. Previously, we demonstrated that van der Waals forces are sufficient for strong adhesion and friction in gecko setae, and that water-based capillary adhesion is not required. However, recent studies demonstrated that adhesion increases with relative humidity (RH) and proposed that surface hydration and capillary water bridge formation is important or even necessary. In this study, we confirmed a significant effect of RH on gecko adhesion, but rejected the capillary adhesion hypothesis. While contact forces of isolated tokay gecko setal arrays increased with humidity, the increase was similar on hydrophobic and hydrophilic surfaces, inconsistent with a capillary mechanism. Contact forces increased with RH even at high shear rates, where capillary bridge formation is too slow to affect adhesion. How then can a humidity-related increase in adhesion and friction be explained? The effect of RH on the mechanical properties of setal ß-keratin has escaped consideration until now. We discovered that an increase in RH softens setae and increases viscoelastic damping, which increases adhesion. Changes in setal materials properties, not capillary forces, fully explain humidity-enhanced adhesion, and van der Waals forces remain the only empirically supported mechanism of adhesion in geckos.

Microscopic modeling of the dynamics of frictional adhesion in the gecko attachment system.

We present a simple microscopic model describing the unique friction behavior of gecko setal arrays as they are dragged on smooth surfaces. Unlike other solids of high elastic modulus that do not stick under van der Waals forces alone, the gecko setal arrays do not require a compressive force to display a drag resistance but rather develop a tensile normal force when they are dragged (J. Experim. Biol. 2006, 209, 3569). We describe this unique behavior with a microscopic model involving curved beam structures at two length scales: at the spatula level, thousands of independent curved beams repeat detachment and reattachment, whereas at the seta level, the curved beam geometry of the seta induces a coupling between the frictional force and the adhesive force that depends on the angle of contact, therefore allowing easy release when the animal needs it. Our model accounts well for the dependence of the drag and adhesion forces on the drag velocity and can also explain macroscopic attachment/ detachment cycles of the setal array.

Role of tilted adhesion fibrils (setae) in the adhesion and locomotion of gecko-like systems.

Geckos are super climbers: they can readily and rapidly stick to almost any surface, whether hydrophilic or hydrophobic, rough or smooth, in dry or wet conditions, and detach with equal rapidity within tens of milliseconds. In this paper, we discuss the rapid switching between the strong adhesion/friction (attached) state and zero adhesion/friction (detached) state, and present a finite element analysis of gecko setae in terms of their adhesion and friction forces. The analysis shows why the asymmetric, naturally curved setae with a directional tilt play a crucial role in the gecko's articulation mechanism, consistent with recent experimental studies of gecko setal arrays. We derive guidelines for designing synthetic versions of gecko adhesive pads, and propose a design for a "gecko-inspired" adhesive surface consisting of arrays of curved, asymmetric, and directionally oriented microfibrils, attached to a semirigid backing, and suggest a method for its actuation.

Frictional and elastic energy in gecko adhesive detachment.

Geckos use millions of adhesive setae on their toes to climb vertical surfaces at speeds of over 1 m s(-1). Climbing presents a significant challenge for an adhesive since it requires both strong attachment and easy, rapid removal. Conventional pressure-sensitive adhesives are either strong and difficult to remove (e.g. duct tape) or weak and easy to remove (e.g. sticky notes). We discovered that the energy required to detach adhering tokay gecko setae (W(d)) is modulated by the angle (theta) of a linear path of detachment. Gecko setae resist detachment when dragged towards the animal during detachment (theta = 30 degrees ) requiring W(d) = 5.0+/-0.86(s.e.) J m(-2) to detach, largely due to frictional losses. This external frictional loss is analogous to viscous internal frictional losses during detachment of pressure-sensitive adhesives. We found that, remarkably, setae possess a built-in release mechanism. Setae acted as springs when loaded in tension during attachment and returned elastic energy when detached along the optimal path (theta=130 degrees ), resulting in W(d) = -0.8+/-0.12 J m(-2). The release of elastic energy from the setal shaft probably causes spontaneous release, suggesting that curved shafts may enable easy detachment in natural, and synthetic, gecko adhesives.

Convergent setal morphology in sand-covering spiders suggests a design principle for particle capture.

Sicarius and Homalonychus are unrelated, desert-dwelling spiders that independently evolved the ability to cover themselves in fine sand particles, making them cryptic against their background. Observations that particles associate with these spiders' setae inspired us to investigate the role of setal microstructure in particle capture and retention. Here we report that Sicarius and Homalonychus convergently evolved numerous high aspect ratio, flexible fibres that we call 'hairlettes' protruding from the setal shaft. We demonstrate that particles attach more densely to regions of Homalonychus with hairlettes than to other regions of the same animal where hairlettes are absent, and document close contact of hairlettes to sand particles that persists after applying force. Mathematical models further suggest that adhesion of hairlettes to sand particles is a sufficient mechanism of particle capture and retention. Together, these data provide the first evidence that hairlettes facilitate sand retention through intermolecular adhesion to particles. Their independent evolutionary origins in Sicarius and Homalonychus suggest that the unique setal structure is adaptive and represents a general biomechanical mechanism for sand capture to cuticle. This discovery has implications for the design of inventions inspired by this system, from camouflage to the management of granular systems.

Analysis of the locomotor activity of a nocturnal desert lizard (Reptilia: Gekkonidae: Teratoscincus scincus) under varying moonlight.

1. This project seeks to identify determinants of the variation observed in the foraging behavior of predatory animals, especially in moonlight, using a lizard as a model. 2. Moonlight generally enhances the foraging efficiency of nocturnal visual predators and often depresses the locomotor activity of prey animals. Previous evidence has indicated for three different nocturnal species of smallish gecko lizards that they respond to moonlight by increasing their activity. 3. In this study some aspects of the foraging activity of the somewhat larger nocturnal psammophilous Teratoscincus scincus, observed near Repetek and Ashgabat, Turkmenistan, were significantly depressed by moonlight, while several confounding factors (sex, maturity, size, sand temperature, hour, prior handling and observer effect) were taken into account. 4. This behavioral difference may relate to the eye size of the various species. 5. Additionally, a novel method of analyzing foraging behavior shows that in this species the duration of moves increases the duration of subsequent stationary pauses. Measurement of locomotor speed, yielding an average speed of 220% of the maximum aerobic speed, indicates a need for these pauses. Secondarily, pause duration decreases the duration of subsequent moves, precluding escalation of move duration. 6. The results of this and related projects advocate the taking into account of physiological and environmental factors that may affect an animal's foraging behavior.

Tempo and mode of performance evolution across multiple independent origins of adhesive toe pads in lizards.

Understanding macroevolutionary dynamics of trait evolution is an important endeavor in evolutionary biology. Ecological opportunity can liberate a trait as it diversifies through trait space, while genetic and selective constraints can limit diversification. While many studies have examined the dynamics of morphological traits, diverse morphological traits may yield the same or similar performance and as performance is often more proximately the target of selection, examining only morphology may give an incomplete understanding of evolutionary dynamics. Here, we ask whether convergent evolution of pad-bearing lizards has followed similar evolutionary dynamics, or whether independent origins are accompanied by unique constraints and selective pressures over macroevolutionary time. We hypothesized that geckos and anoles each have unique evolutionary tempos and modes. Using performance data from 59 species, we modified Brownian motion (BM) and Ornstein-Uhlenbeck (OU) models to account for repeated origins estimated using Bayesian ancestral state reconstructions. We discovered that adhesive performance in geckos evolved in a fashion consistent with Brownian motion with a trend, whereas anoles evolved in bounded performance space consistent with more constrained evolution (an Ornstein-Uhlenbeck model). Our results suggest that convergent phenotypes can have quite distinctive evolutionary patterns, likely as a result of idiosyncratic constraints or ecological opportunities.

Increased capacity for sustained locomotion at low temperature in parthenogenetic geckos of hybrid origin.

The evolution of parthenogenesis is typically associated with hybridization and polyploidy. These correlates of parthenogenesis may have important physiological consequences that need be taken into account in understanding the relative merits of sexual and parthenogenetic reproduction. We compared the thermal sensitivity of aerobically sustained locomotion in hybrid/triploid parthenogenetic races of the gecko Heteronotia binoei and their diploid sexual progenitors. Endurance times at low temperature (10 degrees , 12.5 degrees , and 15 degrees C, 0.05 km h(-1)) were significantly greater in parthenogenetic females than in sexual females. Comparison of oxygen consumption rates during sustained locomotion at increasing speeds (0.05, 0.10, 0.15, 0.20, 0.25, and 0.30 km h(-1), 25 degrees C) indicated that parthenogenetic lizards have higher maximum oxygen consumption rates and maximum aerobic speeds than do female sexual geckos. In addition, parthenogenetic geckos showed greater levels of voluntary activity at 15 degrees C than did sexual geckos, although this pattern appears strongest in comparison to male sexual forms. Parthenogenetic lineages of Heteronotia thus have an advantage over sexual lineages in being capable of greater aerobic activity. This result is opposite of that found in prior studies of parthenogenetic teiid lizards (genus Cnemidophorus) and highlights the idiosyncratic nature of phenotypic evolution in parthenogens of hybrid origin.

Geckoprinting: assembly of microelectronic devices on unconventional surfaces by transfer printing with isolated gecko setal arrays.

Developing electronics in unconventional forms provides opportunities to expand the use of electronics in diverse applications including bio-integrated or implanted electronics. One of the key challenges lies in integrating semiconductor microdevices onto unconventional substrates without glue, high pressure or temperature that may cause damage to microdevices, substrates or interfaces. This paper describes a solution based on natural gecko setal arrays that switch adhesion mechanically on and off, enabling pick and place manipulation of thin microscale semiconductor materials onto diverse surfaces including plants and insects whose surfaces are usually rough and irregular. A demonstration of functional 'geckoprinted' microelectronic devices provides a proof of concept of our results in practical applications.

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.

Macroscale adhesion of gecko setae reflects nanoscale differences in subsurface composition.

Surface energies are commonly used to determine the adhesion forces between materials. However, the component of surface energy derived from long-range forces, such as van der Waals forces, depends on the material's structure below the outermost atomic layers. Previous theoretical results and indirect experimental evidence suggest that the van der Waals energies of subsurface layers will influence interfacial adhesion forces. We discovered that nanometre-scale differences in the oxide layer thickness of silicon wafers result in significant macroscale differences in the adhesion of isolated gecko setal arrays. Si/SiO(2) bilayer materials exhibited stronger adhesion when the SiO(2) layer is thin (approx. 2 nm). To further explore how layered materials influence adhesion, we functionalized similar substrates with an octadecyltrichlorosilane monolayer and again identified a significant influence of the SiO(2) layer thickness on adhesion. Our theoretical calculations describe how variation in the SiO(2) layer thickness produces differences in the van der Waals interaction potential, and these differences are reflected in the adhesion mechanics. Setal arrays used as tribological probes provide the first empirical evidence that the 'subsurface energy' of inhomogeneous materials influences the macroscopic surface forces.

Dry self-cleaning properties of hard and soft fibrillar structures.

Recently, gecko-inspired synthetic adhesives (GSAs) have been made using a variety of fabrication techniques and materials, with one made from a hard polymer having been reported to recover its shear adhesion after fouling by normal use, or "dry self-clean", a feature useful for applications in wall crawling robots, reusable adhesives, microfabrication and solar panel cleaning. This paper investigates the impact of two design parameters on the dry self-cleaning capability of GSAs by experimentally testing two GSAs after fouling with small (1 µm), medium (3-10 µm), and large (40-50 µm) particles. We found that a GSA made from a hard thermoplastic with nanoscopic fibers was able to recover 96-115% of its shear adhesion after fouling with small and large but not medium particles, while a GSA made from a soft polymer and microscopic fibers recovered 40-55% on medium and large particles, with SEM imaging revealing particles embedding within the polymer. An analysis of the contact strength between fibers, particles and substrates of various dimensions and elasticity reveals that dry self-cleaning will be more effective for GSAs fabricated with smaller fiber diameters and for GSAs fabricated from materials with smaller loss functions, such as hard thermoplastics. These results have important implications on the choice of materials and geometries used for GSAs when dry self-cleaning capability is a desired function in the material.

Effects of humidity on the mechanical properties of gecko setae.

We tested the hypothesis that an increase in relative humidity (RH) causes changes in the mechanical properties of the keratin of adhesive gecko foot hairs (setae). We measured the effect of RH on the tensile deformation properties, fracture, and dynamic mechanical response of single isolated tokay gecko setae and strips of the smooth lamellar epidermal layer. The mechanical properties of gecko setae were strongly affected by RH. The complex elastic modulus (measured at 5 Hz) of a single seta at 80% RH was 1.2 GPa, only 39% of the value when dry. An increase in RH reduced the stiffness and increased the strain to failure. The loss tangent increased significantly with humidity, suggesting that water absorption produces a transition to a more viscous type of deformation. The influence of RH on the properties of the smooth epidermal layer was comparable with that of isolated seta, with the exception of stress at rupture. These values were two to four times greater for the setae than for the smooth layer. The changes in mechanical properties of setal keratin were consistent with previously reported increases in contact forces, supporting the hypothesis that an increase in RH softens setal keratin, which increases adhesion and friction.

Rate-dependent frictional adhesion in natural and synthetic gecko setae.

Geckos owe their remarkable stickiness to millions of dry, hard setae on their toes. In this study, we discovered that gecko setae stick more strongly the faster they slide, and do not wear out after 30,000 cycles. This is surprising because friction between dry, hard, macroscopic materials typically decreases at the onset of sliding, and as velocity increases, friction continues to decrease because of a reduction in the number of interfacial contacts, due in part to wear. Gecko setae did not exhibit the decrease in adhesion or friction characteristic of a transition from static to kinetic contact mechanics. Instead, friction and adhesion forces increased at the onset of sliding and continued to increase with shear speed from 500 nm s(-1) to 158 mm s(-1). To explain how apparently fluid-like, wear-free dynamic friction and adhesion occur macroscopically in a dry, hard solid, we proposed a model based on a population of nanoscopic stick-slip events. In the model, contact elements are either in static contact or in the process of slipping to a new static contact. If stick-slip events are uncorrelated, the model further predicted that contact forces should increase to a critical velocity (V*) and then decrease at velocities greater than V*. We hypothesized that, like natural gecko setae, but unlike any conventional adhesive, gecko-like synthetic adhesives (GSAs) could adhere while sliding. To test the generality of our results and the validity of our model, we fabricated a GSA using a hard silicone polymer. While sliding, the GSA exhibited steady-state adhesion and velocity dependence similar to that of gecko setae. Observations at the interface indicated that macroscopically smooth sliding of the GSA emerged from randomly occurring stick-slip events in the population of flexible fibrils, confirming our model predictions.

A microfabricated wedge-shaped adhesive array displaying gecko-like dynamic adhesion, directionality and long lifetime.

Gecko adhesion has become a paradigmatic example of bio-inspired engineering, yet among the many gecko-like synthetic adhesives (GSAs), truly gecko-like performance remains elusive. Many GSAs have previously demonstrated one or two features of the gecko adhesive. We present a new wedge-shaped GSA that exhibits several gecko-like properties simultaneously: directional features; zero force at detachment; high ratio of detachment force to preload force; non-adhesive default state; and the ability to maintain performance while sliding, even after thousands of cycles. Individual wedges independently detach and reattach during sliding, resulting in high levels of shear and normal adhesion during drag. This behaviour provides a non-catastrophic failure mechanism that is desirable for applications such as climbing robots where sudden contact failure would result in serious falls. The effects of scaling patch sizes up to tens of square centimetres are also presented and discussed. Patches of 1 cm(2) had an adhesive pressure of 5.1 kPa while simultaneously supporting 17.0 kPa of shear. After 30 000 attachment/detachment cycles, a patch retained 67 per cent of its initial adhesion and 76 per cent of its initial shear without cleaning. Square-based wedges of 20 mum and 50 mum are manufactured in a moulding process where moulds are fabricated using a dual-side, dual-angle lithography process on quartz wafers with SU-8 photoresist as the mould material and polydimethylsiloxane as the cast material.

Gecko adhesion pad: a smart surface?

Recently, it has been shown that humidity can increase the adhesion of the spatula pads that form the outermost (adhesive) surface of the tokay gecko feet by 50% relative to the main adhesion mechanism (i.e. van der Waals adhesive forces), although the mechanism by which the enhancement is realized is still not well understood. A change in the surface hydrophobicity of a gecko setal array is observed when the array, which supports the spatulae, is exposed to a water drop for more than 20 min, suggesting a change in the hydrophilic-lyophilic balance (HLB), and therefore of the conformation of the surface proteins. A surface force apparatus (SFA) was used to quantify these changes, i.e. in the adhesion and friction forces, while shearing the setal array against a silica surface under (i) dry conditions, (ii) 100% humidity and (iii) when fully immersed in water. The adhesion increased in the humid environment but greatly diminished in water. Although the adhesion forces changed significantly, the friction forces remained unaffected, indicating that the friction between these highly textured surfaces is 'load-controlled' rather than 'adhesion-controlled'. These results demonstrate that the gecko adhesive pads have the ability to exploit environmental conditions to maximize their adhesion and stabilize their friction forces. Future designs of synthetic dry adhesives inspired by the gecko can potentially include similar 'smart' surfaces that adapt to their environment.

Gecko adhesion: evolutionary nanotechnology.

If geckos had not evolved, it is possible that humans would never have invented adhesive nanostructures. Geckos use millions of adhesive setae on their toes to climb vertical surfaces at speeds of over 1ms-1. Climbing presents a significant challenge for an adhesive in requiring both strong attachment and easy rapid removal. Conventional pressure-sensitive adhesives (PSAs) are either strong and difficult to remove (e.g. duct tape) or weak and easy to remove (e.g. sticky notes). The gecko adhesive differs dramatically from conventional adhesives. Conventional PSAs are soft viscoelastic polymers that degrade, foul, self-adhere and attach accidentally to inappropriate surfaces. In contrast, gecko toes bear angled arrays of branched, hair-like setae formed from stiff, hydrophobic keratin that act as a bed of angled springs with similar effective elastic modulus to that of PSAs. Setae are self-cleaning and maintain function for months during repeated use in dirty conditions. Setae are an anisotropic 'frictional adhesive' in that adhesion requires maintenance of a proximally directed shear load, enabling either a tough bond or spontaneous detachment. Gecko-like synthetic adhesives may become the glue of the future-and perhaps the screw of the future as well.