Physical constraints lead to parallel evolution of micro- and nanostructures of animal adhesive pads: a review

Abstract

Adhesive pads are functional systems with specific micro- and nanostructures which evolved as a response to specific environmental conditions and therefore exhibit convergent traits. The functional constraints that shape systems for the attachment to a surface are general requirements. Different strategies to solve similar problems often follow similar physical principles, hence, the morphology of attachment devices is affected by physical constraints. This resulted in two main types of attachment devices in animals: hairy and smooth. They differ in morphology and ultrastructure but achieve mechanical adaptation to substrates with different roughness and maximise the actual contact area with them. Species-specific environmental surface conditions resulted in different solutions for the specific ecological surroundings of different animals. As the conditions are similar in discrete environments unrelated to the group of animals, the micro- and nanostructural adaptations of the attachment systems of different animal groups reveal similar mechanisms. Consequently, similar attachment organs evolved in a convergent manner and different attachment solutions can occur within closely related lineages. In this review, we present a summary of the literature on structural and functional principles of attachment pads with a special focus on insects, describe micro- and nanostructures, surface patterns, origin of different pads and their evolution, discuss the material properties (elasticity, viscoelasticity, adhesion, friction) and basic physical forces contributing to adhesion, show the influence of different factors, such as substrate roughness and pad stiffness, on contact forces, and review the chemical composition of pad fluids, which is an important component of an adhesive function. Attachment systems are omnipresent in animals. We show parallel evolution of attachment structures on micro- and nanoscales at different phylogenetic levels, focus on insects as the largest animal group on earth, and subsequently zoom into the attachment pads of the stick and leaf insects (Phasmatodea) to explore convergent evolution of attachment pads at even smaller scales. Since convergent events might be potentially interesting for engineers as a kind of optimal solution by nature, the biomimetic implications of the discussed results are briefly presented.

Louse flies holding on mammals' hair: Comparative functional morphology of specialized attachment devices of ectoparasites (Diptera: Hippoboscoidea)

“…To move on thicker hairs, the parasites need to use a different attachment solution. Solitary coat hairs could be pushed against the fifth tarsomere by the claws and therefore captured by the pulvilli, which provide adhesion on more or less planar surfaces (S. N. Gorb, 2005; Büscher and Gorb, 2021; Figure 7b).…”

Attachment Performance of Stick Insects (Phasmatodea) on Plant Leaves with Different Surface Characteristics

“…The two pads work in complementary directions: the arolium provides adhesion to the substrate and the euplantulae generate friction due to shear forces when pressed onto the surface. The combination of these pads and the adjustability of the amount of involved euplantulae results in a highly adaptive attachment system [ 25 , 26 , 27 , 28 , 29 , 30 ]. While the arolium of Phasmatodea is usually smooth, the euplantulae show a high diversity of microscopic surface structures [ 25 ], most likely to adapt best to the corresponding substrate conditions prevailing in different habitats.…”

“…While the arolium of Phasmatodea is usually smooth, the euplantulae show a high diversity of microscopic surface structures [ 25 ], most likely to adapt best to the corresponding substrate conditions prevailing in different habitats. The most common microstructures are smooth and nubby, whereas other euplantula microstructures are characterized by different pattering and aspect ratios resulting in several potential functions, such as frictional anisotropy, randomization of pattern directionality and coping with water or particular contaminations [ 25 , 28 , 29 ]. The adhesion and traction of the nubby and smooth euplantulae have already been experimentally tested on artificial surfaces with different roughness.…”

Gripping performance in the stick insect Sungaya inexpectata in dependence on the pretarsal architecture

“…On either much smaller or much larger feature sizes of the substrate surface, their performance quickly diminishes (Song et al 2016). Phasmatodean pretarsal adhesive pads (arolia) mainly interact with smooth surfaces, where they are able to form an intimate contact and by this enhance adhesion and friction (Büscher and Gorb 2021). They always generate a certain degree of attachment, but are mainly used on surfaces, where the claws do not find grip on, by this effectively extending the range of substrates for locomotion (Song et al 2016).…”