Dataset Information

Elastic modulus of tree frog adhesive toe pads.

ABSTRACT: Previous work using an atomic force microscope in nanoindenter mode indicated that the outer, 10- to 15-?m 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.

SUBMITTER: Barnes WJ

PROVIDER: S-EPMC3176399 | biostudies-literature | 2011 Oct

REPOSITORIES: biostudies-literature

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Elastic modulus of tree frog adhesive toe pads.

Barnes W Jon P WJ Goodwyn Pablo J Perez PJ Nokhbatolfoghahai Mohsen M Gorb Stanislav N SN

Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology 20110612 10

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 o ...[more]

PMID: 21667266

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Project description: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.

Project description:BackgroundMany 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 findingsWe 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.SignificanceThis 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.

Dataset Information

Elastic modulus of tree frog adhesive toe pads.

Publications

Elastic modulus of tree frog adhesive toe pads.

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