Stiff skin, soft core: soft backings enhance the conformability and friction of fibre-reinforced adhesives.

Biomimetic adhesives with a stiff fibre-reinforced base layer generate strong attachment, even without bioinspired micropatterning of the contact surface. However, current fibre-reinforced adhesive designs are still less versatile with respect to substrate variability than their biological counterparts. In this study, we enhance the comformability of a fibre-reinforced adhesive on curved substrates by adding bioinspired soft backings. We designed and fabricated soft backing variations (polyurethane foams and silicone hydroskeletons) with varying compressive stiffnesses that mimic the soft viscoelastic structures in the adhesive appendages of tree frogs, geckos and other animals. The backings were mounted on a smooth silicone layer enforced with a polyester mesh, and we experimentally investigated the contact area and friction performance of these adhesives on a curved substrate. The results show that the contact area and friction created by a fibre-reinforced adhesive with a soft backing in contact with a non-flat substrate scale inversely with backing stiffness. The integration of stiff fibre-reinforcement with a compressible backing represents an important step in bringing bioinspired adhesives out of the laboratory and into the real world, for example in soft robotic grippers. Moreover, our findings stimulate further research into the role of soft tissues in biological adhesive systems.

Studying Stickiness: Methods, Trade-Offs, and Perspectives in Measuring Reversible Biological Adhesion and Friction.

Controlled, reversible attachment is widely spread throughout the animal kingdom: from ticks to tree frogs, whose weights span from 2 mg to 200 g, and from geckos to mosquitoes, who stick under vastly different situations, such as quickly climbing trees and stealthily landing on human hosts. A fascinating and complex interplay of adhesive and frictional forces forms the foundation of attachment of these highly diverse systems to various substrates. In this review, we present an overview of the techniques used to quantify the adhesion and friction of terrestrial animals, with the aim of informing future studies on the fundamentals of bioadhesion, and motivating the development and adoption of new or alternative measurement techniques. We classify existing methods with respect to the forces they measure, including magnitude and source, i.e., generated by the whole body, single limbs, or by sub-structures. Additionally, we compare their versatility, specifically what parameters can be measured, controlled, and varied. This approach reveals critical trade-offs of bioadhesion measurement techniques. Beyond stimulating future studies on evolutionary and physicochemical aspects of bioadhesion, understanding the fundamentals of biological attachment is key to the development of biomimetic technologies, from soft robotic grippers to gentle surgical tools.

Design of Tree-Frog-Inspired Adhesives.

The adhesive toe pads of tree frogs have inspired the design of various so-called 'smooth' synthetic adhesives for wet environments. However, these adhesives do not reach the attachment performance of their biological models in terms of contact formation, maintenance of attachment, and detachment. In tree frogs, attachment is facilitated by an interconnected ensemble of superficial and internal morphological components, which together form a functional unit. To help bridging the gap between biological and bioinspired adhesives, in this review, we (1) provide an overview of the functional components of tree frog toe pads, (2) investigate which of these components (and attachment mechanisms implemented therein) have already been transferred into synthetic adhesives, and (3) highlight functional analogies between existing synthetic adhesives and tree frogs regarding the fundamental mechanisms of attachment. We found that most existing tree-frog-inspired adhesives mimic the micropatterned surface of the ventral epidermis of frog pads. Geometrical and material properties differ between these synthetic adhesives and their biological model, which indicates similarity in appearance rather than function. Important internal functional components such as fiber-reinforcement and muscle fibers for attachment control have not been considered in the design of tree-frog-inspired adhesives. Experimental work on tree-frog-inspired adhesives suggests that the micropatterning of adhesives with low-aspect-ratio pillars enables crack arresting and the drainage of interstitial liquids, which both facilitate the generation of van der Waals forces. Our analysis of experimental work on tree-frog-inspired adhesives indicates that interstitial liquids such as the mucus secreted by tree frogs play a role in detachment. Based on these findings, we provide suggestions for the future design of biomimetic adhesives. Specifically, we propose to implement internal fiber-reinforcements inspired by the fibrous structures in frog pads to create mechanically reinforced soft adhesives for high-load applications. Contractile components may stimulate the design of actuated synthetic adhesives with fine-tunable control of attachment strength. An integrative approach is needed for the design of tree-frog-inspired adhesives that are functionally analogous with their biological paradigm.

Comparative and functional analysis of the digital mucus glands and secretions of tree frogs.

BACKGROUND: Mucus and mucus glands are important features of the amphibian cutis. In tree frogs, the mucus glands and their secretions are crucial components of the adhesive digital pads of these animals. Despite a variety of hypothesised functions of these components in tree frog attachment, the functional morphology of the digital mucus glands and the chemistry of the digital mucus are barely known. Here, we use an interdisciplinary comparative approach to analyse these components, and discuss their roles in tree frog attachment. RESULTS: Using synchrotron micro-computer-tomography, we discovered in the arboreal frog Hyla cinerea that the ventral digital mucus glands differ in their morphology from regular anuran mucus glands and form a subdermal gland cluster. We show the presence of this gland cluster also in several other-not exclusively arboreal-anuran families. Using cryo-histochemistry as well as infrared and sum frequency generation spectroscopy on the mucus of two arboreal (H. cinerea and Osteopilus septentrionalis) and of two terrestrial, non-climbing frog species (Pyxicephalus adspersus and Ceratophrys cranwelli), we find neutral and acidic polysaccharides, and indications for proteinaceous and lipid-like mucus components. The mucus chemistry varies only little between dorsal and ventral digital mucus in H. cinerea, ventral digital and abdominal mucus in H. cinerea and O. septentrionalis, and between the ventral abdominal mucus of all four studied species. CONCLUSIONS: The presence of a digital mucus gland cluster in various anuran families, as well as the absence of differences in the mucus chemistry between arboreal and non-arboreal frog species indicate an adaptation towards generic functional requirements as well as to attachment-related requirements. Overall, this study contributes to the understanding of the role of glands and their secretions in tree frog attachment and in bioadhesion in general, as well as the evolution of anurans.

Estimating the maximum attachment performance of tree frogs on rough substrates.

Tree frogs can attach to smooth and rough substrates using their adhesive toe pads. We present the results of an experimental investigation of tree frog attachment to rough substrates, and of the role of mechanical interlocking between superficial toe pad structures and substrate asperities in the tree frog species Litoria caerulea and Hyla cinerea. Using a rotation platform setup, we quantified the adhesive and frictional attachment performance of whole frogs clinging to smooth, micro-, and macrorough substrates. The transparent substrates enabled quantification of the instantaneous contact area during detachment by using frustrated total internal reflection. A linear mixed-effects model shows that the adhesive performance of the pads does not differ significantly with roughness (for nominal roughness levels of 0-15 µm) in both species. This indicates that mechanical interlocking does not contribute to the attachment of whole animals. Our results show that the adhesion performance of tree frogs is higher than reported previously, emphasising the biomimetic potential of tree frog attachment. Overall, our findings contribute to a better understanding of the complex interplay of attachment mechanisms in the toe pads of tree frogs, which may promote future designs of tree-frog-inspired adhesives.

Force-transmitting structures in the digital pads of the tree frog Hyla cinerea: a functional interpretation.

The morphology of the digital pads of tree frogs is adapted towards attachment, allowing these animals to attach to various substrates and to explore their arboreal habitat. Previous descriptions and functional interpretations of the pad morphology mostly focussed on the surface of the ventral epidermis, and little is known about the internal pad morphology and its functional relevance in attachment. In this study, we combine histology and synchrotron micro-computer-tomography to obtain a comprehensive 3-D morphological characterisation of the digital pads (in particular of the internal structures involved in the transmission of attachment forces from the ventral pad surface towards the phalanges) of the tree frog Hyla cinerea. A collagenous septum runs from the distal tip of the distal phalanx to the ventral cutis and compartmentalises the subcutaneous pad volume into a distal lymph space and a proximal space, which contains mucus glands opening via long ducts to the ventral pad surface. A collagen layer connects the ventral basement membrane via interphalangeal ligaments with the middle phalanx. The collagen fibres forming this layer curve around the transverse pad-axis and form laterally separated ridges below the gland space. The topological optimisation of a shear-loaded pad model using finite element analysis (FEA) shows that the curved collagen fibres are oriented along the trajectories of the maximum principal stresses, and the optimisation also results in ridge-formation, suggesting that the collagen layer is adapted towards a high stiffness during shear loading. We also show that the collagen layer is strong, with an estimated tensile strength of 2.0-6.5 N. Together with longitudinally skewed tonofibrils in the superficial epidermis, these features support our hypothesis that the digital pads of tree frogs are primarily adapted towards the generation and transmission of friction rather than adhesion forces. Moreover, we generate (based on a simplified FEA model and predictions from analytical models) the hypothesis that dorsodistal pulling on the collagen septum facilitates proximal peeling of the pad and that the septum is an adaptation towards detachment rather than attachment. Lastly, by using immunohistochemistry, we (re-)discovered bundles of smooth muscle fibres in the digital pads of tree frogs. We hypothesise that these fibres allow the control of (i) contact stresses at the pad-substrate interface and peeling, (ii) mucus secretion, (iii) shock-absorbing properties of the pad, and (iv) the macroscopic contact geometry of the ventral pad surface. Further work is needed to conclude on the role of the muscular structures in tree frog attachment. Overall, our study contributes to the functional understanding of tree frog attachment, hence offering novel perspectives on the ecology, phylogeny and evolution of anurans, as well as the design of tree-frog-inspired adhesives for technological applications.

Tree frog attachment: mechanisms, challenges, and perspectives.

Tree frogs have the remarkable ability to attach to smooth, rough, dry, and wet surfaces using their versatile toe pads. Tree frog attachment involves the secretion of mucus into the pad-substrate gap, requiring adaptations towards mucus drainage and pad lubrication. Here, we present an overview of tree frog attachment, with focus on (i) the morphology and material of the toe pad; (ii) the functional demands on the toe pad arising from ecology, lifestyle, and phylogenetics; (iii) experimental data of attachment performance such as adhesion and friction forces; and (iv) potential perspectives on future developments in the field. By revisiting reported data and observations, we discuss the involved mechanisms of attachment and propose new hypotheses for further research. Among others, we address the following questions: Do capillary and hydrodynamic forces explain the strong friction of the toe pads directly, or indirectly by promoting dry attachment mechanisms? If friction primarily relies on van der Waals (vdW) forces instead, how much do these forces contribute to adhesion in the wet environment tree frogs live in and what role does the mucus play? We show that both pad morphology and measured attachment performance suggest the coaction of several attachment mechanisms (e.g. capillary and hydrodynamic adhesion, mechanical interlocking, and vdW forces) with situation-dependent relative importance. Current analytical models of capillary and hydrodynamic adhesion, caused by the secreted mucus and by environmental liquids, do not capture the contributions of these mechanisms in a comprehensive and accurate way. We argue that the soft pad material and a hierarchical surface pattern on the ventral pad surface enhance the effective contact area and facilitate gap-closure by macro- to nanoscopic drainage of interstitial liquids, which may give rise to a significant contribution of vdW interactions to tree frog attachment. Increasing the comprehension of the complex mechanism of tree frog attachment contributes to a better understanding of other biological attachment systems (e.g. in geckos and insects) and is expected to stimulate the development of a wide array of bioinspired adhesive applications.