Ultrastructure and physical properties of an adhesive surface, the toe pad epithelium of the tree frog, Litoria caerulea White

Abstract

SUMMARYKnowledge of both surface structure and physical properties such as stiffness and elasticity are essential to understanding any adhesive system. In this study of an adhesion surface in the tree frog, Litoria caerulea White, a variety of techniques including atomic force microscopy were used to investigate the microstructure and properties of an epithelium that adheres through wet adhesion. Litoria toe pads consist of a hexagonal array of flat-topped epithelial cells, separated by mucus-filled channels. Under an atomic force microscope, this ʻflatʼ surface is highly structured at the nanoscale, consisting of a tightly packed array of columnar nanopillars (described as hemidesmosomes by previous authors), 326±84 nm in diameter, each of which possesses a central dimple 8±4 nm in depth. In fixed tissue (transmission electron microscopy), the nanopillars are approximately as tall as they are broad. At the gross anatomical level, larger toe pads may be subdivided into medial and lateral parts by two large grooves. Although the whole toe pad is soft and easily deformable, the epithelium itself has an effective elastic modulus equivalent to silicon rubber (mean E eff =14.4±20.9 MPa; median E eff =5.7 MPa), as measured by the atomic force microscope in nanoindentation mode. The functions of these structures are discussed in terms of maximising adhesive and frictional forces by conforming closely to surface irregularities at different length scales and maintaining an extremely thin fluid layer between pad and substrate. The biomimetic implications of these findings are reviewed.

Sticking like sticky tape: tree frogs use friction forces to enhance attachment on overhanging surfaces

“…Indeed, our estimate, based on microindentation, does not account for either the presence of bone or cartilage that extends almost to the end of the digits or the fact that the outer cell layer is relatively stiff because it is highly keratinized. This keratinization gives a Young's modulus in the range 5-15 MPa, as measured by nanoindentation using an atomic force microscope [56]. Indeed, a much better fit to our force data is produced by using an elastic modulus of E ¼ 500 kPa (see dashed red line in figure 6).…”

Biomimetics: lessons from nature–an overview

“…Tree frog toe attachment pads consist of a hexagonal array of flat-topped epidermal cells of approximately 10 mm in size separated by approximately 1 mm wide mucus-filled channels; the flattened surface of each cell consists of a submicrometre array of nanopillars or pegs of approximately 100-400 nm diameter (figure 21). The toe pads are made of an extremely soft, inhomogeneous material; the epithelium itself has an effective elastic modulus of approximately 15 MPa, equivalent to silicone rubber (Scholz et al 2009). The pads are permanently wetted by mucus secreted from glands that open into the channels between epidermal cells.…”

Morphological studies of the toe pads of the rock frog,Staurois parvus(family: Ranidae) and their relevance to the development of new biomimetically inspired reversible adhesives

“…Additionally, on surfaces wetted by rain, the channels may act to disperse excess fluid to the pad edge. Finally, the epithelial cells are covered by a dense array of nanopillars [23] that originate from desmosomes [12]. Within the epithelial cells, there are large numbers of keratin fibrils (tonofilaments), arising from the nanopillars, that are oriented approximately normal to the surface [12,20].…”