Plant surfaces with cuticular folds are slippery for beetles

Abstract

Plant surfaces covered with three-dimensional (3D) waxes are known to strongly reduce insect adhesion, leading to slippery surfaces. Besides 3D epicuticular waxes, cuticular folds are a common microstructure found on plant surfaces, which have not been quantitatively investigated with regard to their influence on insect adhesion. We performed traction experiments with Colorado potato beetles on five plant surfaces with cuticular folds of different magnitude. For comparison, we also tested (i) smooth plant surfaces and (ii) plant surfaces possessing 3D epicuticular waxes. Traction forces on surfaces with medium cuticular folds, of about 0.5 µm in both height and thickness and a spacing of 0.5-1.5 µm, were reduced by an average of 88 per cent in comparison to smooth plant surfaces. Traction forces were reduced by the same order of magnitude as on plant surfaces covered with 3D epicuticular waxes. For surface characterization, we performed static contact angle measurements, which proved a strong effect of cuticular folds also on surface wettability. Surfaces possessing cuticular folds of greater magnitude showed higher contact angles up to superhydrophobicity. We hypothesize that cuticular folds reduce insect adhesion mainly due to a critical roughness, reducing the real contact area between the surface and the insect's adhesive devices.

Figure 1.

Experimental setup: the traction force of an actively walking beetle, being attracted by a small light, was recorded using a highly sensitive force transducer. AD, transducer amplifier and AD converter; PC, laptop for data acquisition; F, highly sensitive force transducer; H, hair; W, beeswax; B, beetle; S, plant surface; L, light source; ST, stage. (Online version in colour.)

Figure 2.

SEM micrographs of plant surfaces with different types of structuring. (a,b) Smooth surfaces covered only with 2D layers or crusts of wax: (a) Magnolia grandiflora (adaxial leaf surface) and (b) Ilex aquifolium (adaxial leaf surface); (c) low cuticular folds: Litchi chinensis (adaxial leaf surface); (d,e) medium cuticular folds: (d) Hevea brasiliensis (adaxial leaf surface) and (e) Cyclamen persicum (petal leaf surface); (f) high cuticular folds: Hevea brasiliensis (abaxial leaf surface); (g) hierarchical surface with cuticular folds: Litchi chinensis (abaxial leaf surface); (h) 3D epicuticular waxes: Diospyros kaki (fruit surface). Scale bars, 20 µm. Insets show pictures of droplets of 5 µl of double-distilled water on the respective plant surface used for calculating the contact angles.

Figure 3.

SEM micrographs of the attachment devices in a male Leptinotarsa decemlineata. (a) Lateral view and (b) ventral view of a hind-leg. (c) Individual claw tip. Tarsal adhesive setae of the (d) filamentous, (e) lanceolate, (f) spatula-shaped and (g) discoidal type (latter found in males only). Setae are termed according to Voigt et al. [22], with setae of the filamentous and lanceolate type being grouped as tapered setae. M, setae of discoidal type; S, spatula-shaped setae; T, tapered setae.

Figure 4.

Traction forces of actively walking male Leptinotarsa decemlineata beetles on plant surfaces relative to traction forces on glass (box–whisker plot). Comparison of different surface structuring with cuticular folds of different magnitude to plant surfaces showing 3D epicuticular waxes and smooth plant surfaces without cuticular folds. Results of statistical analysis (nested ANOVA and Tukey HSD post hoc tests) are based on log-transformed data. Significant differences between groups are indicated by lower case letters. Upper case letters indicate significant differences between individual plant species. (Online version in colour.)

Figure 5.

Static contact angles of water droplets on plant surfaces with cuticular folds of different dimensions compared to plant surfaces showing 3D epicuticular waxes and smooth plant surfaces (box–whisker plot). The grey lines at 90° and 150° indicate the limit from hydrophilic to hydrophobic and from hydrophobic to superhydrophobic surfaces according to Koch et al. [2]. Results of statistical analysis (nested ANOVA and Tukey HSD post hoc tests) are based on square-transformed data. Significant differences between groups are indicated by lower case letters. Upper case letters indicate significant differences between individual plant species. (Online version in colour.)