Light and electron microscopic analyses of the high deformability of adhesive toe pads in White's tree frog, Litoria caerulea

Abstract

White's tree frog (Litoria caerulea) has large, adhesive toe pads that are among the softest of all known biological structures. To explore the morphological basis for the physical properties of the toe pads, the internal microstructure of the toe pads in L. caerulea was examined using both light and transmission electron microscopy. Three design elements that are distinct from other areas of skin were observed. First, the keratinocytes comprising the adhesive surface of the toe pad all contained keratin filament bundles (tonofibrils) exhibiting structural anisotropy. Specifically, the curved conformation of the hierarchical (branching) tonofibrils was characterized by the formation of anastomoses consisting of tonofibrils beneath the adhesive cell surface and stem keratin filament bundles concentrated in the lower-middle part of the dorsal-side of adhesive cells. Second, the cytoplasm of keratinocytes in the most superficial cell layer contained glycoproteins (stained by periodic acid/Schiff reagent) that are considered to confer high viscoelasticity. Third, the dermis contained large lymph spaces interspersed with elastic fibers and collagen fibers, which were relatively sparsely distributed compared to the dorsal skin of the toe pads. The profiles of these structures were easily deformed by the slight application of pressure. These findings reaffirmed that the unique internal architecture of the toe pads in L. caerulea contributed to their remarkable softness and high deformability, which in turn increased the contact area and provided improved adaptability to the local topography of natural surfaces. J. Morphol. 277:1509-1516, 2016. © 2016 Wiley Periodicals, Inc.

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

“…Overall, the epidermal morphology found in this study agrees with the extensive description for the same species by Ernst (). The presence of skewed cells in the second most apical layer of epidermal cells in Hyla cinerea (this study), Litoria caerulea (Nakano & Saino, ) and Staurois parvus (Drotlef et al. ) contradicts cell skewing to be a mere age effect, as suggested previously (Schuberg, ; Ernst, ).…”

“…Overall, the epidermal morphology found in this study agrees with the extensive description for the same species by Ernst (1973a). The presence of skewed cells in the second most apical layer of epidermal cells in Hyla cinerea (this study), Litoria caerulea (Nakano & Saino, 2016) and Staurois parvus (Drotlef et al 2015) contradicts cell skewing to be a mere age effect, as suggested previously (Schuberg, 1891;Ernst, 1973a). We hypothesise that the longitudinally skewed tonofibrils increase the stiffness of the apical epidermis during the transmission of shear loads deeper into the digital pad, possibly increasing friction by the distribution of mechanical stresses over a larger volume of pad material (Xue et al 2017) and maintaining the structural integrity of the epidermal surface.…”

“…The dermal and subcutaneous structures in the digital pads of tree frogs have received little attention in previous research. To our knowledge, the latest reported efforts to analyse the internal morphology of the pads were made 90 years ago (Noble & Jaeckle, 1928), while later studies focussed on bony and cartilaginous structures (Paukstis & Brown, 1991;Manzano et al 2007;Kamermans & Vences, 2009) and the superficial epidermis (Ernst, 1973a;Green, 1979;Green & Simon, 1986;Hertwig & Sinsch, 1995;Mizuhira, 2004;Scholz et al 2009;Barnes et al 2013;Nokhbatolfoghahai, 2013;Chakraborti et al 2014a,b;Drotlef et al 2015;Nakano & Saino, 2016). Overall, we find a number of tissues that were until now undescribed or have been characterised only partially.…”

“…,b; Drotlef et al. ; Nakano & Saino, ). Overall, we find a number of tissues that were until now undescribed or have been characterised only partially.…”

“…The dense ‘sponge‐like’ network of tonofibrils within the apical regions of the superficial cells may locally increase the mechanical resilience of the epidermis surface (Drotlef et al. ; Nakano & Saino, ). Moreover, the skewed tonofibrils may help to increase the pad‐substrate contact area and adhesion during proximal pulling of the pad (Drotlef et al.…”