Impact of cell shape in hierarchically structured plant surfaces on the attachment of male Colorado potato beetles (Leptinotarsa decemlineata)

Abstract

Plant surfaces showing hierarchical structuring are frequently found in plant organs such as leaves, petals, fruits and stems. In our study we focus on the level of cell shape and on the level of superimposed microstructuring, leading to hierarchical surfaces if both levels are present. While it has been shown that epicuticular wax crystals and cuticular folds strongly reduce insect attachment, and that smooth papillate epidermal cells in petals improve the grip of pollinators, the impact of hierarchical surface structuring of plant surfaces possessing convex or papillate cells on insect attachment remains unclear. We performed traction experiments with male Colorado potato beetles on nine different plant surfaces with different structures. The selected plant surfaces showed epidermal cells with either tabular, convex or papillate cell shape, covered either with flat films of wax, epicuticular wax crystals or with cuticular folds. On surfaces possessing either superimposed wax crystals or cuticular folds we found traction forces to be almost one order of magnitude lower than on surfaces covered only with flat films of wax. Independent of superimposed microstructures we found that convex and papillate epidermal cell shapes slightly enhance the attachment ability of the beetles. Thus, in plant surfaces, cell shape and superimposed microstructuring yield contrary effects on the attachment of the Colorado potato beetle, with convex or papillate cells enhancing attachment and both wax crystals or cuticular folds reducing attachment. However, the overall magnitude of traction force mainly depends on the presence or absence of superimposed microstructuring.

Keywords: cuticular folds; epicuticular wax crystals; insect–plant interaction; papillae; structure–function relationship.

Figure 1

Plant surfaces investigated showing different types of structuring. Pictograms on the top show the shape of the epidermal cells: Tabular cells (i), convex cells (ii) and papillate cells (iii). Pictograms on the left illustrate the level of superimposed microstructuring: Films of wax / no further structuring (o), epicuticular wax crystals (wc) and cuticular folds (cf). SEM micrographs of plant surfaces: (a) Magnolia grandiflora, (b) Paeonia officinalis, (c) Calathea zebrina, (d) Diospyros kaki, (e) Paeonia suffruticosa, (f) Colocasia esculenta, (g) Hevea brasiliensis, (h) Vitis vinifera, (i) Rosa hybrid Floribunda cv. “Sarabande”.

Figure 2

Traction forces of actively walking male Leptinotarsa decemlineata beetles on plant surfaces of different structure, both on the cellular level and on the level of superimposed microstructuring. Significant differences in traction force between tabular, convex and papillate epidermal cells are indicated by lower case letters. M. gra: Magnolia grandiflora; P. off: Paeonia officinalis; C. zeb.: Calathea zebrina, D. kaki: Diospyros kaki, P. suff.: Paeonia suffruticosa , C. esc.: Colocasia esculenta, H. bras.: Hevea brasiliensis, V. vin.: Vitis vinifera, Rosa: Rosa hybrid Floribunda cv. “Sarabande”.

Figure 3

SEM micrographs of the attachment devices in a male Leptinotarsa decemlineata. (a) Ventral view of a hind leg; (b) claw tip; (c–f): Tarsal adhesive setae: (c) filamentous, (d) lanceolate, (e) spatula-shaped and (f) discoidal setae. Terminology according to Voigt et al. [13]. Adapted from [8].

Figure 4

Experimental setup. Traction forces of a beetle (b) actively walking on a plant surface (p) were recorded by using a highly sensitive force transducer (f). The beetle was fixed to the force transducer by a piece of hair (h) and attracted by a small light source (l). Adapted from [8].