Sticking under wet conditions: the remarkable attachment abilities of the torrent frog, staurois guttatus

Tree frogs climb smooth surfaces utilising capillary forces arising from an air-fluid interface around their toe pads, whereas torrent frogs are able to climb in wet environments near waterfalls where the integrity of the meniscus is at risk. This study compares the adhesive capabilities of a torrent frog to a tree frog, investigating possible adaptations for adhesion under wet conditions. We challenged both frog species to cling to a platform which could be tilted from the horizontal to an upside-down orientation, testing the frogs on different levels of roughness and water flow. On dry, smooth surfaces, both frog species stayed attached to overhanging slopes equally well. In contrast, under both low and high flow rate conditions, the torrent frogs performed significantly better, even adhering under conditions where their toe pads were submerged in water, abolishing the meniscus that underlies capillarity. Using a transparent platform where areas of contact are illuminated, we measured the contact area of frogs during platform rotation under dry conditions. Both frog species not only used the contact area of their pads to adhere, but also large parts of their belly and thigh skin. In the tree frogs, the belly and thighs often detached on steeper slopes, whereas the torrent frogs increased the use of these areas as the slope angle increased. Probing small areas of the different skin parts with a force transducer revealed that forces declined significantly in wet conditions, with only minor differences between the frog species. The superior abilities of the torrent frogs were thus due to the large contact area they used on steep, overhanging surfaces. SEM images revealed slightly elongated cells in the periphery of the toe pads in the torrent frogs, with straightened channels in between them which could facilitate drainage of excess fluid underneath the pad

Attachment performance of male tree frogs (<i>R. pardalis</i>) and male and female torrent frogs (<i>S. guttatus</i>) on the 1125 mm rough surface at a high flow rate.

<p>Male data are from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073810#pone-0073810-g003" target="_blank">Figure 3</a>. Angles of fall for female torrent frogs are significantly higher than those of male tree frogs (Mann-Whitney U-test, ), but lower than those of male torrent frogs (Mann Whitney U-test, ).</p

Frog species used in this study.

<p>Males of the (A) Harlequin Tree Frog (<i>R. pardalis</i>) and (B) the Black-spotted Rock Frog (<i>S. guttatus</i>) in their natural habitats.</p

Scanning electron micrographs of toe pad epithelia in different frog species.

<p>(A) the tree frog <i>R. pardalis</i>, (B) the torrent frog <i>S. guttatus</i> near the edge of pad, and (C) the torrent frog, <i>Odorrana hosii</i>. White solid lines illustrate shortest routes to the edge of pad. White dashed lines are routes across the pad. Arrows show examples of the pointed ends of the epithelial cells of <i>O. hosii</i>. Scale bars: 20 μm.</p

Diagram of the key elements of the tilting platform.

<p>Not drawn to scale.</p

Masses and lengths of the two species used in the experiments.

<p>Masses and lengths of the two species used in the experiments.</p

Scanning electron micrographs of ventral body skin.

<p>Belly (A,B) and ventral thigh epithelium (C,D) of the tree frog (<i>R. pardalis</i>, left column) and the torrent frog (<i>S. guttatus</i>, right column). Insets show structures at higher magnification.</p

Attachment performance of the two frog species under varying conditions.

<p>Comparison of (A) slip angles and (B) fall angles between the tree frog (<i>Rhacophorus pardalis</i>) and the torrent frog (<i>Staurois guttatus</i>) on different wet (‘low’& ‘high’flow rate) and rough surfaces. The details of the statistical tests between the two frog species are listed in Tables S4 and S6 in Supplementary Materials. Intraspecific differences of frog performance on both different surfaces and under different flow regimes are listed in Tables S1 to S3 and S5 in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073810#pone.0073810.s002" target="_blank">Supplementary Materials S1</a>.</p

Contact areas of the two frog species at 5 tilting positions.

<p>Using a special illumination technique (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073810#s2" target="_blank">Materials and Methods</a>), the contact area of ventral body parts (toe pads, belly, thighs and uncategorised areas) of (A) the tree frog (<i>R. pardalis</i>) and (B) the torrent frog (<i>S. guttatus</i>) was measured at 0°, 45°, 90°, 135° and 180°. The photos at the top are images of the frogs at horizontal (0°) and inverted (180°) tilting positions. The plots represent medians of 42 trials from 6 frogs (tree frogs) and 33 trials from 6 frogs (torrent frogs), the percentages at the top representing the proportion of frogs still attached at each tilt angle.).</p

Friction and Adhesion forces per area of different body parts.

<p>Statistical differences are denoted as follows: ‘*’ , ‘**’: , ‘n.s.’: not significant.</p