Wet but not slippery: Boundary friction in tree frog adhesive toe pads

Abstract

Tree frogs are remarkable for their capacity to cling to smooth surfaces using large toe pads. The adhesive skin of tree frog toe pads is characterized by peg-studded hexagonal cells separated by deep channels into which mucus glands open. The pads are completely wetted with watery mucus, which led previous authors to suggest that attachment is solely due to capillary and viscous forces generated by the fluid-filled joint between the pad and the substrate. Here, we present evidence from single-toe force measurements, laser tweezer microrheometry of pad mucus and interference reflection microscopy of the contact zone in Litoria caerulea, that tree frog attachment forces are significantly enhanced by close contacts and boundary friction between the pad epidermis and the substrate, facilitated by the highly regular pad microstructure.

Figure 1

Morphology of tree frog toe pads. (a) White's tree frog (Litoria caerulea). (b–d) SEMs of (b) toe pad, (c) epidermis with hexagonal epithelial cells and (d) high power view of the surface of a single hexagonal cell showing peg-like projections. (e) TEM of cross-section through cell surface.

Figure 2

In vivo analysis of Litoria caerulea toe pad contact with glass using interference reflection microscopy (IRM). (a–c) Corresponding images of the same area of the contact zone taken using different wavelengths and illuminating numerical apertures (INA): (a) 546 nm, INA=0.27, (b) 436 nm, INA=0.27, and (c) 546 nm, INA=1.27. Note the hemidesmosome pegs visible as dark spots in the central cell areas. Asterisks denote one epidermal cell, which is not in close contact (h≥40 nm) and has a convex shape. (d), Intensity profile along the arrow shown in (a) and (b). Arrows indicate the position of the second order ‘green’ minimum coinciding with the second order ‘blue’ maximum. (e) Reconstruction of the fluid film thickness along the arrow shown in (a) and (b) (see appendix B). (f) Frequency of measured fluid film thicknesses in hexagons with zero order minimum (n=87 from five frogs).

Figure 3

Microrheology of Litoria caerulea toe pad mucus using laser tweezers. (a) Bead displacement elicited by sinusoidal fluid movement at three different frequencies. (b) Sinusoidal fit of bead and fluid (=substrate) movement. Here, bead displacement was phase-shifted by 87.0° against the movement of the fluid. (c) Relationship of bead displacement amplitude and velocity (frequency) measured for toe pad mucus and pure water. The slopes indicate that this sample of toe pad mucus was 1.65 times more viscous than water.

Figure 4

Shear stress measurement in single toe pads of Litoria caerulea. (a) Friction force during a sliding experiment consisting of 20 s sliding toward the body (500 μm s⁻¹) followed by 2 min standstill. (b) Toe pad shear stress at the transition from rest to sliding (‘onset’), during steady sliding (‘sliding’) and 2 min after the end of the motor movement (‘remaining’). Centre lines denote medians; boxes, the inner two quartiles; and whiskers, the upper and lower 5%. Data from 10 toe pads of three frogs.