Silk secretion from tarantula feet revisited: alleged spigots are probably chemoreceptors.

Controversial views have been expressed about whether tarantula feet can secrete fine silk threads that could prevent them from falling off smooth vertical surfaces. Two studies have claimed that 'ribbed hairs' on the tarsi of tarantulas produce silk. We examined these ribbed hairs in several tarantula species using light and scanning electron microscopy, and compared them with the silk-producing spigots on the abdominal spinnerets. We found that, morphologically, these ribbed hairs correspond very closely to known chemosensitive hairs in spiders; they have a distinct socket, a bent hair shaft with fine cuticular ridges, an eccentric double lumen within the hair shaft, and a blunt tip with a subterminal pore. Spigots on the spinnerets have a large bulbous base instead of a socket, a long shaft with a scaly surface and a central terminal pore. We never observed any silk threads coming out of these ribbed hairs under the electron microscope. By contrast, silk threads exiting the spigots on the spinnerets were common. Interestingly, ribbed hairs also occur on the spinnerets, often side by side with the silk-producing spigots. Our conclusion is that the ribbed hairs are chemoreceptors, not spigots. Observations of live tarantulas clinging inverted to glass coverslips confirmed that some substance is produced by the ribbed hairs, but it remains unclear whether this secretion is actually silk. In any case, the thousands of adhesive setae on the tarsi of legs and pedipalps almost certainly far outweigh any potential contribution from the sparsely distributed trails secreted by the ribbed hairs.

Terrestrial locomotion in arachnids.

In this review, we assess the current state of knowledge on terrestrial locomotion in Arachnida. Arachnids represent a single diverse (>100,000 species) clade containing well-defined subgroups (at both the order and subordinal levels) that vary morphologically around a basic body plan, yet exhibit highly disparate limb usage, running performance, and tarsal attachment mechanisms. Spiders (Araneae), scorpions (Scorpiones), and harvestmen (Opiliones) have received the most attention in the literature, while some orders have never been subject to rigorous mechanical characterization. Most well-characterized taxa move with gaits analogous to the alternating tripod gaits that characterize fast-moving Insecta - alternating tetrapods or alternating tripods (when one pair of legs is lifted from the ground for some other function). However, between taxa, there is considerable variation in the regularity of phasing between legs. Both large and small spiders appear to show a large amount of variation in the distribution of foot-ground contact, even between consecutive step-cycles of a single run. Mechanisms for attachment to vertical surfaces also vary, and may depend on tufts of adhesive hairs, fluid adhesives, silks, or a combination of these. We conclude that Arachnida, particularly with improvements in microelectronic force sensing technology, can serve as a powerful study system for understanding the kinematics, dynamics, and ecological correlates of sprawled-posture locomotion.

Arachnids secrete a fluid over their adhesive pads.

BACKGROUND: Many arachnids possess adhesive pads on their feet that help them climb smooth surfaces and capture prey. Spider and gecko adhesives have converged on a branched, hairy structure, which theoretically allows them to adhere solely by dry (solid-solid) intermolecular interactions. Indeed, the consensus in the literature is that spiders and their smooth-padded relatives, the solifugids, adhere without the aid of a secretion. METHODOLOGY AND PRINCIPAL FINDINGS: We investigated the adhesive contact zone of living spiders, solifugids and mites using interference reflection microscopy, which allows the detection of thin liquid films. Like insects, all the arachnids we studied left behind hydrophobic fluid footprints on glass (mean refractive index: 1.48-1.50; contact angle: 3.7-11.2°). Fluid was not always secreted continuously, suggesting that pads can function in both wet and dry modes. We measured the attachment forces of single adhesive setae from tarantulas (Grammostola rosea) by attaching them to a bending beam with a known spring constant and filming the resulting deflection. Individual spider setae showed a lower static friction at rest (26%±2.8 SE of the peak friction) than single gecko setae (Thecadactylus rapicauda; 96%±1.7 SE). This may be explained by the fact that spider setae continued to release fluid after isolation from the animal, lubricating the contact zone. SIGNIFICANCE: This finding implies that tarsal secretions occur within all major groups of terrestrial arthropods with adhesive pads. The presence of liquid in an adhesive contact zone has important consequences for attachment performance, improving adhesion to rough surfaces and introducing rate-dependent effects. Our results leave geckos and anoles as the only known representatives of truly dry adhesive pads in nature. Engineers seeking biological inspiration for synthetic adhesives should consider whether model species with fluid secretions are appropriate to their design goals.

Orientation angle and the adhesion of single gecko setae.

We investigated the effects of orientation angle on the adhesion of single gecko setae using dual-axis microelectromechanical systems force sensors to simultaneously detect normal and shear force components. Adhesion was highly sensitive to the pitch angle between the substrate and the seta's stalk. Maximum lateral adhesive force was observed with the stalk parallel to the substrate, and adhesion decreased smoothly with increasing pitch. The roll orientation angle only needed to be roughly correct with the spatular tuft of the seta oriented grossly towards the substrate for high adhesion. Also, detailed measurements were made to control for the effect of normal preload forces. Higher normal preload forces caused modest enhancement of the observed lateral adhesive force, provided that adequate contact was made between the seta and the substrate. These results should be useful in the design and manufacture of gecko-inspired synthetic adhesives with anisotropic properties, an area of substantial recent research efforts.

Functional demands of dynamic biological adhesion: an integrative approach.

Climbing organisms are constantly challenged to make their way rapidly and reliably across varied and often novel terrain. A diversity of morphologically and mechanically disparate attachment strategies have evolved across widely distributed phylogenetic groups to aid legged animals in scaling these surfaces, notable among them some very impressive adhesive pads. Despite the differences between, for example, the dry fibrillar pads of geckos and the smooth, secretion-aided pads of stick insects, I hypothesize that they face similar functional demands in their environment. I outline three broad criteria defining dynamic biological adhesion: reusability, reversibility, and substrate tolerance. Organismal adhesive pads must be able to attach repeatedly without significant decline in performance, detach easily at will, and adhere strongly to the broadest possible range of surfaces in their habitat. A survey of the literature suggests that evidence for these general principles can be found in existing research, but that many gaps remain to be filled. By taking a comparative, integrative approach to biological dynamic adhesion, rather than focusing on a few model organisms, investigators will continue to discover new and interesting attachment strategies in natural systems.

Subdigital setae of narrow-toed geckos, including a Eublepharid (Aeluroscalabotes felinus).

Subdigital adhesive setae have previously been documented in all legged gecko families except the Eublepharidae. I present evidence that members of Aeluroscalabotes felinus, the only arboreal eublepharids, possess subdigital setae up to 9 mum in length. This discovery suggests that the conditions leading to adhesive setae were probably present in the ancestors of all geckos, rather than arising multiple times within Gekkota. The digits and setae of Aeluroscalabotes resemble those of other climbing, bent-toed geckos. I describe the setal morphology of the following bent-toed species: Cyrtodactylus peguensis, Gonatodes albogularis, and Pristurus rupestris. The presence of subdigital setae is highly correlated with an arboreal lifestyle across geckos and other lizards such as anoles and skinks. Although relatively simple in form, these setae likely confer additional traction that significantly benefits climbing species. Further developmental and biomechanical studies comparing these species with more agile climbers like the Tokay will improve our understanding of the evolutionary processes leading to adhesive setae, and consequently inform engineers attempting to fabricate effective artificial gecko setae.

Ancestrally high elastic modulus of gecko setal beta-keratin.

Typical bulk adhesives are characterized by soft, tacky materials with elastic moduli well below 1MPa. Geckos possess subdigital adhesives composed mostly of beta-keratin, a relatively stiff material. Biological adhesives like those of geckos have inspired empirical and modelling research which predicts that even stiff materials can be effective adhesives if they take on a fibrillar form. The molecular structure of beta-keratin is highly conserved across birds and reptiles, suggesting that material properties of gecko setae should be similar to that of beta-keratin previously measured in birds, but this has yet to be established. We used a resonance technique to measure elastic bending modulus in two species of gecko from disparate habitats. We found no significant difference in elastic modulus between Gekko gecko (1.6 GPa +/- 0.15s.e.; n=24 setae) and Ptyodactylus hasselquistii (1.4 GPa +/- 0.15s.e.; n=24 setae). If the elastic modulus of setal keratin is conserved across species, it would suggest a design constraint that must be compensated for structurally, and possibly explain the remarkable variation in gecko adhesive morphology.

Evidence for van der Waals adhesion in gecko setae.

Geckos have evolved one of the most versatile and effective adhesives known. The mechanism of dry adhesion in the millions of setae on the toes of geckos has been the focus of scientific study for over a century. We provide the first direct experimental evidence for dry adhesion of gecko setae by van der Waals forces, and reject the use of mechanisms relying on high surface polarity, including capillary adhesion. The toes of live Tokay geckos were highly hydrophobic, and adhered equally well to strongly hydrophobic and strongly hydrophilic, polarizable surfaces. Adhesion of a single isolated gecko seta was equally effective on the hydrophobic and hydrophilic surfaces of a microelectro-mechanical systems force sensor. A van der Waals mechanism implies that the remarkable adhesive properties of gecko setae are merely a result of the size and shape of the tips, and are not strongly affected by surface chemistry. Theory predicts greater adhesive forces simply from subdividing setae to increase surface density, and suggests a possible design principle underlying the repeated, convergent evolution of dry adhesive microstructures in gecko, anoles, skinks, and insects. Estimates using a standard adhesion model and our measured forces come remarkably close to predicting the tip size of Tokay gecko seta. We verified the dependence on size and not surface type by using physical models of setal tips nanofabricated from two different materials. Both artificial setal tips stuck as predicted and provide a path to manufacturing the first dry, adhesive microstructures.

Mechanisms of adhesion in geckos.

The extraordinary adhesive capabilities of geckos have challenged explanation for millennia, since Aristotle first recorded his observations. We have discovered many of the secrets of gecko adhesion, yet the millions of dry, adhesive setae on the toes of geckos continue to generate puzzling new questions and valuable answers. Each epidermally-derived, keratinous seta ends in hundreds of 200 nm spatular tips, permitting intimate contact with rough and smooth surfaces alike. Prior studies suggested that adhesive force in gecko setae was directly proportional to the water droplet contact angle (θ) , an indicator of the free surface energy of a substrate. In contrast, new theory suggests that adhesion energy between a gecko seta and a surface (W(GS)) is in fact proportional to (1 + cosθ), and only for θ > 60°. A reanalysis of prior data, in combination with our recent study, support the van der Waals hypothesis of gecko adhesion, and contradict surface hydrophobicity as a predictor of adhesion force. Previously, we and our collaborators measured the force production of a single seta. Initial efforts to attach a seta failed because of improper 3D orientation. However, by simulating the dynamics of gecko limbs during climbing (based on force plate data) we discovered that, in single setae, a small normal preload, combined with a 5 µm displacement yielded a very large adhesive force of 200 microNewton (µN), 10 times that predicted by whole-animal measurements. 6.5 million setae of a single tokay gecko attached maximally could generate 130 kg force. This raises the question of how geckos manage to detach their feet in just 15 ms. We discovered that simply increasing the angle that the setal shaft makes with the substrate to 30° causes detachment. Understanding how simultaneous attachment and release of millions of setae are controlled will require an approach that integrates levels ranging from molecules to lizards.