Entrapment of bed bugs by leaf trichomes inspires microfabrication of biomimetic surfaces

Abstract

Resurgence in bed bug infestations and widespread pesticide resistance have greatly renewed interest in the development of more sustainable, environmentally friendly methods to manage bed bugs. Historically, in Eastern Europe, bed bugs were entrapped by leaves from bean plants, which were then destroyed; this purely physical entrapment was related to microscopic hooked hairs (trichomes) on the leaf surfaces. Using scanning electron microscopy and videography, we documented the capture mechanism: the physical impaling of bed bug feet (tarsi) by these trichomes. This is distinct from a Velcro-like mechanism of non-piercing entanglement, which only momentarily holds the bug without sustained capture. Struggling, trapped bed bugs are impaled by trichomes on several legs and are unable to free themselves. Only specific, mechanically vulnerable locations on the bug tarsi are pierced by the trichomes, which are located at effective heights and orientations for bed bug entrapment despite a lack of any evolutionary association. Using bean leaves as templates, we microfabricated surfaces indistinguishable in geometry from the real leaves, including the trichomes, using polymers with material properties similar to plant cell walls. These synthetic surfaces snag the bed bugs temporarily but do not hinder their locomotion as effectively as real leaves.

Figure 1.

Bed bug standing on a kidney bean leaf. (a) Lower magnification image. (b) LV-SEM image of a hind leg of a bed bug (yellow) showing its size relative to the microscopic trichomes (green), which surround the tarsi.

Figure 2.

(a) Fabrication of biomimetic surfaces from bean leaves. (1–3) A negative moulding material is poured onto a leaf surface, and pressure is applied. (4–6) The leaf is removed, and the negative mould is filled with the positive replica material. (7) The negative mould is removed leaving the replica. (b,c) LV-SEM images of the bean leaf show the surface density of trichomes and the recurved, sharp trichome tips. (d,e) SEM images of the replicate materials appear identical to the natural leaves.

Figure 3.

LV-SEM images of bed bug legs (yellow) on bean leaf surfaces with hooked trichomes (green). (a) Piercing under a pretarsal claw leads to entrapment of a bug by a leaf. (b) Piercing occasionally occurs at a tarsal intersegmental membrane, also causing entrapment of a bug. (c) Higher magnification of piercing from (a). (d) In contrast, hooking causes momentary snagging of a bug leg.

Figure 4.

Underside of a bed bug tarsus showing a dangling broken trichome (highlighted in green) as evidence of piercing. Note that the trichome stalk is hollow.

Figure 5.

SEM image of a cross section of negative moulding material showing an embedded natural trichome tip (highlighted in green) that broke off the natural leaf trichome during moulding. Natural tips similar to this were sometimes incorporated into hybrid microfabricated surfaces.

Figure 6.

Discrimination between natural (hybrid) and synthetic trichome tips on microfabricated surfaces using elemental analysis was possible using energy dispersive X-ray spectroscopy (EDS). (a) An LV-SEM image of a trichome on a natural bean leaf surface and the locations of EDS spectra are identified. The trichome tip (a1) shows a strong silicon signature compared with the base (a2) and leaf surface (a3). (b) An SEM image showing both a hybrid trichome (b1) and non-hybrid trichome (b2) and their corresponding EDS spectra showing the presence or the absence of detectable silicon, respectively. (c) EDS mapping of trichomes on the leaf surface showing the presence of silicon on the natural trichomes. (d) Representative synthetic surface showing examples of natural trichome tips incorporated into the polymer surface (indicated by the presence of silicon) along with an example of a fully synthetic trichome (indicated by a circle).