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Biological Fibrillar Adhesives: Functional Principles and Biomimetic Applications

  • Stanislav N. GorbEmail author
  • Lars Heepe
Living reference work entry

Abstract

Specific mechanisms of adhesion found in nature are discussed in the previous chapter (chapter “Bioadhesives”). One of the most discussed biological systems in the last decade are the so-called fibrillar adhesives of insects, spiders, and geckos. These systems are adapted for dynamic adhesion of animals during locomotion and, therefore, have some extraordinary properties, such as (1) directionality, (2) preload by shear, (3) quick detachment by peeling, (4) low dependence on the substrate chemistry, (5) reduced ability to contamination and self-cleaning, and (6) the absence or strong reduction of self-adhesion. In the present chapter, we review functional principles of such biological systems in various animal groups with an emphasis on insects and discuss their biomimetic potential. The data on ultrastructure and mechanics of materials of adhesive pads, movements during contact formation and breakage, the role of the fluid in the contact between the pad and substrate are presented here. The main goal is to demonstrate how a comparative experimental approach in studies of biological systems aids in the development of novel adhesive materials and systems. The microstructured adhesive systems, inspired by studies of biological systems of insects, spiders, and geckos, are also shortly reviewed.

Keywords

Attachment Biomimetics Bioinspired surfaces Microstructure Fibrillar adhesives Dry adhesives Dynamic adhesion Reversible adhesion Bioadhesion Microfabrication Gecko Insect Spider 

1 Introduction

Representatives of several animal groups, such as insects, arachnids, tree frogs, and lizards, are able to attach to and walk on smooth vertical surfaces and even on the ceiling (reviews by Gorb 2001; Scherge and Gorb 2001; Autumn 2006; Wolff and Gorb 2016). This ability is due to highly specialized attachment devices located at different parts of their legs. Biomimetic transfer of such systems into industrial applications is a very challenging task, and several working groups of materials scientists worldwide are currently attempting to reach this goal by applying various approaches of microfabrication and surface science in general. However, biological systems are far too complex for copying them exactly. That is why intensive structural and experimental comparative studies are required to find out which structural and mechanical features of real biological systems are essential for biomimetics. In order to understand functional principles of animal attachment devices, it is not enough to have information about external morphology of the structures. An integrative approach is necessary to combine data on ultrastructure and mechanical properties of materials, arrangement of muscles, joint design, movements during contact formation and breakage (motor control), sensorics, forces and their directionality, contact mechanics at micro- and nanoscale, potential substrates (surface profile and surface energy), and the presence and properties of the fluid in the contact between the pad and the substrate (chemical composition, viscosity, transporting system).

Two important questions have to be answered in order to select the right biological prototype for particular technological requirements. The first question is which product has to be developed, and the second one is which biological system possesses the ability we are going to mimic. Normally, the first and most important requirement from the industry of adhesives is that the new material has to be as sticky as possible. If this is the only requirement, one has to select a prototype among animals and plants using glue-like systems for permanent or long-term adhesion to the substrate (for review, see Gorb 2009 and this book chapter “Bioadhesives”). However, if the requirement for the new material is its ability to allow multiple adhesive cycles, for example, in robotic applications for robot locomotion on smooth walls and the ceiling, with the ability (1) to build and break the contact as fast as possible, (2) to attach to unpredictable surfaces, (3) to have lifetime of millions of attachment-detachment cycles, and (4) to not attach to itself, then we definitely have to search for prototypes among locomotory attachment devices of animals.

To understand principles, at which biological systems operate, detailed studies on ultrastructure, material properties, force range, and motion pattern during locomotion are necessary. Such studies became possible during the last years, because of new developments (1) in microscopical visualization techniques (atomic force microscopy, freezing and environmental scanning electron microscopy), (2) in the characterization of mechanical properties of biological materials and structures in situ and in vivo (measurements of stiffness, hardness, adhesion, friction) at local and global scales, and (3) in computer simulations.

In general, there are two different working strategies that aid in extracting structural and mechanical features of biological objects for further development of bioinspired systems. The first strategy deals with a careful detailed characterization of one particular biological system defined as a model object (one of the most prominent examples for fibrillar adhesives is the gecko toe). The second strategy is focused on a comparative study of a large variety of biological objects, which possess similar functional systems that appeared independently in the course of biological evolution. In our opinion, the second approach is more promising for biomimetics, because structural similarities, which evolved independently in different lineages of organisms, may indicate some kind of “optimal” solution for this type of system. Moreover, a comparative approach aids in extracting essential features and abandoning less important ones for designing artificial prototypes. Although different, these two approaches are complementary and help in the course of the biomimetic process.

Figure 1 provides a summary and categorization of essential features that contribute to the so-called gecko effect. In this chapter, along with this categorization, we report on our 15-year-long experience in studies of locomotory attachment devices in various animal groups with an emphasis on insects. The main goal is to demonstrate how a comparative experimental biological approach can aid in understanding biological attachment systems and derive design rules for the development of novel adhesive materials and systems.
Fig. 1

Summary and categorization of essential features that contribute to the so-called gecko effect: physical mechanisms, attachment pad structure, material and surface properties, and locomotion control. Various substrate properties and environmental factors may influence the adhesive performance of climbing animals (Adapted from Heepe and Gorb 2014. Photo copyright by Alex Mortillaro)

2 Dynamic Adhesion for Locomotion

The adhesive contact between the leg and the substrate is mostly important for a rather short period of time of the stance phase and must be released during the swing phase (Fig. 2). These phases repeat infinitely in step cycles during locomotion. Therefore, adhesive structures of animal legs must fulfill several tasks, sometimes opposite to each other and reversibly executed in repeated step cycles (Gladun et al. 2009). (1) The sticky surface of the leg must be ready to immediately build adhesive contact with the substrate. The contact formation must be fast and established with minimal load on the ceiling. (2) Adhesion of few legs must be strong enough to hold the animal on the inclined and even on the overhanging substrate (reliability). (3) At the same time, adhesion must be low enough to allow smooth and quick detachment of the swinging leg. In other words, adhesion must be reversible. (4) The adhesive surface of the pad must be sticky enough to generate sufficient adhesive force to the substrate, but it should be secured from adhering to itself, to prevent disability of the adhesive surface for the next step cycle.
Fig. 2

Ceiling situation. If the mass m of the animal is in the center of gravity, then its weight is W = m g, the angle of the ground reaction is α, the normal pull-off force component is F n , and the shear force component is F s . Thus, the weight of the animal walking on the ceiling should be counterbalanced by two forces: friction (F f ), which prevents leg sliding along the substrate, and adhesion (F a ), which prevents leg separation from the substrate. In order to walk on the ceiling, it is not sufficient just to generate strong adhesive bond between the leg and substrate. Two additional problems have to be solved: (1) contact formation must be fast, reliable, and performed with the minimal load on the ceiling and (2) contact must be released in the fast manner and with the minimum of the applied load (From Gladun et al. 2009)

3 Pad Structure

To date, both the morphological and ultrastructural bases of the ability of animals to dynamically adhere to vertical surfaces have been studied in detail only in representatives of selected taxa, including insects (reviews by Gorb 2001, 2005; Federle 2006), arachnids (Homann 1957; Kesel et al. 2003; Niederegger and Gorb 2006; Wolff and Gorb 2016), tree frogs (Barnes 2006; Smith et al. 2006), and lizards (Hiller 1968; Autumn 2000, 2002; Huber, 1995a, b). In their evolution, animals have developed two distinctly different mechanisms to attach themselves to a variety of substrates: smooth pads and fibrillar (hairy, setose) pads. Due to the flexibility of the material of the attachment pads or fine surface outgrowths, both mechanisms can maximize the possible contact area with a wide range of substrate profiles (Gorb and Beutel 2001; Gorb 2005).

Interestingly, in different lineages, both types of attachment pads can be found. For example, within insects, such groups as orthopterans, hymenopterans, and thysanopterans bear smooth pads, whereas dipterans, coleopterans, and dermapterans possess mainly fibrillar pads. Within arachnids, representatives of Solifugae have smooth pads, whereas Araneae are characterized by fibrillar ones. Among reptiles, Gekkonidae and Anolinae have fibrillar pads, and some skinks have smooth ones. Additionally, these highly specialized structures are not restricted to one particular area of the leg. For example, in insects, they may be located on claws, derivatives of the pretarsus, tarsal apex, tarsomeres, or tibia. Recent phylogenetic analyses of hexapods based on the pad characters, processed together with characters of other organ systems, aided in resolving the question of the attachment pad evolution in hexapods and showed that these structures have evolved several times, independently (Gorb and Beutel 2001; Beutel and Gorb 2001, 2006).

Fibrillar systems always contain cuticle protuberances on their surfaces (Fig. 3). Protuberances on the fibrillar pads of Coleoptera, Dermaptera, and Diptera belong to different types. Representatives of the first two lineages have socketed setae originating each from two different cells. Setae range in their length from a few micrometers to several millimeters. Dipteran outgrowths are acanthae: single sclerotized protuberances originating from a single cell (Richards and Richards 1979). Structural features of adhesive outgrowths have been previously reported, for example, for flies, the acanthae are hollow inside (Bauchhenss 1979), and some of them contain pores under the terminal plate (Gorb 1998). These pores, presumably, deliver an adhesive secretion directly in the contact area. Pore canals at the base of the shaft may additionally transport secretions to the surface. In beetles, the setal bases are embedded in rubberlike material, which provides flexibility to the supporting material and helps the seta to adapt to various surface profiles.
Fig. 3

Wet fibrillar adhesive system of the fly (ac) and dry fibrillar adhesive system of gecko (dg). (b, c, e, g) Scanning electron microscopy images of adhesive setae. Both systems are similar according to the contact mechanics but differ in relative contribution of different physical forces to the overall adhesion. Insect mainly employ wetting phenomena, whereas gecko system is dominated by intermolecular van der Waals forces

Gecko setae are multibranched, hierarchical structures of 80–100 μm in length (Ruibal and Ernst 1965; Stork 1983; Schleich and Kastle 1986; Roll 1995; Huber et al. 2005a; Rizzo et al. 2006). In anole lizards, setae are smaller and unbranched (ca. 20 μm long) (Ruibal and Ernst 1965; Stork 1983; Rizzo et al. 2006). The gecko setae are not hollow inside. They are formed by proteinaceous fibrils held together by a matrix and surrounded by a proteinaceous sheath. Ordered protein constituent in these structures exhibits a diffraction pattern characteristic of β-keratin. Raman microscopy of individual setae, however, shows the presence of additional protein constituents, some of which may be identified as α-keratins (Rizzo et al. 2006). In anoles, setae emerge from the oberhautchen layer of the epidermal shedding complex into the cells of the clear layer, which act as templates for their growth (Alibardi 1997). The clear layer cells template the formation of spatular terminal elements. This means that setae are fully formed prior to shedding of the external epidermis during the shedding cycle.

4 Nature of Attractive Forces

There are two different adhesive mechanisms in fibrillar systems: a wet one, primarily based on capillarity, and a dry one, primarily based on intermolecular van der Waals interactions. Wet adhesive systems (insects) generate a thin fluid layer in the contact between single hairs and substrate, whereas dry ones (spiders, geckos) do not. Pad fluids have been previously reported from fibrillar pads of reduviid bugs (Edwards and Tarkanian 1970), flies (Bauchhenss 1979; Walker et al. 1985), coccinellid (Ishii 1987; Kosaki and Yamaoka 1996), and chrysomelid (Eisner and Aneshansley 2000) beetles. The pad secretion contains nonvolatile, lipid-like substances that can be observed in footprints stained with Sudan Black. Microscopy data combined with gas chromatography and mass spectrometry showed that secretion of smooth pads of ants and locusts is an emulsion containing water-soluble and lipid-soluble fractions (Federle et al. 2002; Vötsch et al. 2002). For fibrillar pads, two chemically different secretion compositions were reported. Tarsal secretions of beetles were mainly lipid based (Geiselhardt et al. 2009, 2010; Betz 2010) with a small water fraction, whereas in flies it is assumed to be a mainly water-based microemulsion (Gorb 2001) with low lipid content. Footprints of secretion in flies, visualized by cryo-SEM, indicate as well an emulsion-like composition (Fig. 4). Detailed fluid evaporation measurements in beetles Coccinella septempunctata and flies Calliphora vicina by atomic force microscopy supported these observations (Langer et al. 2004; Peisker and Gorb 2012). In flies, a larger volatile fraction was observed, if compared to beetles (Peisker and Gorb 2012). This result is also reflected in the corresponding viscosities of tarsal secretions in flies and beetles. For flies (C. vicina) a viscosity of approximately 11 mPa⋅s was measured by microrheological technique, whereas for beetles (C. septempunctata) it was two times higher, and a viscosity of approximately 22 mPa⋅s was found (Fig. 5) (Peisker et al. 2014). Both secretions showed a Newtonian behavior.
Fig. 4

Fluid in wet fibrillar systems. (a, b) Tenent setae of the syrphid fly Episyrphus balteatus bearing lumen (LU) filled with the fluid and pores (black arrows) under platelike terminal contact elements (PL). (c) Pattern of microdroplets left by the fly Calliphora vicina on the glass surface, as viewed in phase contrast light microscope. (d, e) Same droplets frozen and further replicated with carbon-platinum coating technique and visualized in transmission electron microscope (black arrow indicates direction of coating). Please note pattern of nanodrops on the surface of major droplets. (f, g) Menisci formed around single terminal contact elements of the setae of the fly C. vicina. Fly leg was frozen in contact with smooth glass, carefully removed, and the fluid residues are viewed in cryo-SEM ((a, b) From Gorb 1998. ce From Gorb 2001. (f, g) From Gorb 2007))

Fig. 5

Plots of the mean square displacement (MSD) over the lag time for different fluids (Adapted from Peisker et al. 2014). (a) Dependence of the MSD on lag time (see black line with slope 1) for water (blue dots), the fly fluid (black dots), and the beetle fluid (red dots). The linear relationship in the log-log scale indicates purely viscous (Newtonian) properties of all fluids studied. For the fly and the beetle, all measurements were averaged. Representative MSDs for (b) water, (c) beetle fluid, and (d) fly fluid. Black solid lines are the MSD data points; the gray-shaded area is the standard deviation in each MSD data point; the white-dashed lines are linear fits to the data

In wet fibrillar systems, numerous experiments showed that the main contribution of attractive forces to the overall adhesion is due to capillarity. When hairy pads of the bug Rhodnius prolixus were treated with organic solvents, attachment was impaired (Edwards and Tarkanian 1970). Experiments with freely walking beetles strongly suggested that cohesive forces, surface tension, and molecular adhesion, mediated by the pad secretion, may be involved in the mechanism of attachment (Stork 1980a). Multiple local force-volume measurements, carried out on individual terminal plates of the setae of the fly C. vicina by application of atomic force microscopy (Langer et al. 2004), showed that adhesion strongly decreases as the volume of the secretion decreases, indicating that a layer of pad secretion covering the terminal plates is crucial for the generation of strong attractive force. These data provide direct evidence that, beside van der Waals forces, also attractive capillary forces, mediated by the pad secretion, contribute to the fly’s attachment mechanism (Langer et al. 2004). Similarly, for beetles, traction force experiments on nanoporous plant (Gorb and Gorb 2002) and nanoporous artificial surfaces (Gorb et al. 2010), capable of adsorbing tarsal secretions, showed strong minimization of attachment ability.

In the hairy attachment system of gekkonid lizards, van der Waals interactions are responsible for the generation of attractive forces (Hiller 1968; Autumn et al. 2000, 2002). Experiments, in which the force-displacement curves were determined for individual spatulae by atomic force microscopy, showed that these smallest elements of the gecko’s attachment devices generate forces of about 10 nN. An estimate of adhesion energy (γ) from Kendall’s classical peeling theory (Kendall 1975), which describes the force required to peel a tape of certain width (200 nm for gecko spatula) from a rigid substrate in perpendicular direction, gives γ = 50 mJ•m−2 (Huber et al. 2005a). This value corresponds well to the range expected for adhesion by intermolecular forces (10–100 mJ•m−2; Israelachvili 1992). Using this value of adhesion energy, we may estimate the order of the theoretical force a gecko can produce, assuming all spatulae readily make intimate contact with the substrate and peel off simultaneously. Assuming an effective total peeling line, which is the sum of widths of all spatulae, of 1.8 km for the tokay gecko (Varenberg et al. 2010) and a peeling angle of 30°, shown to be the critical angle of detachment for gecko setae (Autumn et al. 2000), we obtain a maximum force of order 700 N or correspondingly a maximum supported weight of order 70 kg. This large value indicates that only small portions of spatulae are needed in contact with the substrate at each single step. While these estimates show that van der Waals forces can account for the measured adhesion, we cannot unambiguously exclude contributions from capillary forces (Huber et al. 2005b).

5 Multiple Contacts

Based on the studies of different animal groups, an interesting correlation between the setal density and animal weight was found: the heavier the animal, the smaller and more densely packed are the terminal contact elements (Scherge and Gorb 2001) (Fig. 6). Using contact mechanics theories, this scaling effect was explained by applying the principle of contact splitting to the Johnson–Kendall–Roberts (JKR) contact theory (Johnson et al. 1971), according to which splitting up the contact into finer subcontacts increases adhesion on any substrate profile (Arzt et al. 2003). This relationship holds because animals cannot increase the area of the attachment devices proportionally to the body weight due to the different scaling rules for mass and surface area. Therefore, the increase of the attachment strength in hairy systems is realized by increasing the number of single contact points, i.e., by increasing the hair density. It has been shown later that this trend is different within each single lineage of organisms (Peattie and Full 2007). However, a closer look at the terminal contact elements in biological hairy adhesive systems involved in locomotion revealed that they are predominately spatula shaped (Gorb and Varenberg 2007) and cardinally differ from flat-punch- or hemisphere-ended structures (Fig. 7). Therefore, the application of the contact splitting principle to Kendall’s peeling model (Kendall 1975) also provides a proper explanation of multiple contact geometry with spatula-like terminal elements. It demonstrates that an animal’s attachment ability grows with an overall length of the peeling line, which is the sum of widths of all thin-film elements participating in contact (Fig. 8). This robust principle is found to manifest itself across eight orders of magnitude in an overall peeling line ranging from 64 μm for a little red spider mite to 1.8 km for a tokay gecko, generalizing the critical role of spatulate terminal elements in biological fibrillar adhesion (Varenberg et al. 2010).
Fig. 6

Dependence of the contact density of terminal contacts on the body mass in fibrillar pad systems in representatives from diverse animal groups: 1, 2, 4, 5, flies; 3, beetle; 6, bug; 7, spider; 8, gekkonid lizards (Adapted from Scherge and Gorb 2001). The systems, located above solid horizontal line, preferably rely on van der Waals forces (dry adhesion), whereas other ones mostly rely on capillary and viscose forces (wet adhesion))

Fig. 7

Cryo-SEM images of spatula-shaped thin-film terminal elements while in contact with smooth glass, in hairy attachment pads found in animals of evolutionary remote lineages. (a) Beetle (Gastrophysa viridula). (b) Fly (Calliphora vicina). (c) Spider (Cupiennius salei). (d) Tokay gecko (Gekko gecko). Arrows point in distal direction (From Varenberg et al. 2010)

Fig. 8

Graphical representation of the effect of adhesion enhancement by increasing the peeling line length. (a) A single piece of elastic film peeling from a rigid substrate. Peeling force F is proportional to the film width b (at constant peel angle θ for given pair of materials). (b) A series of elastic films covering the same contact area as in (a). Peeling force F s is threefold the value F in (a) due to an overall growth of the peeling line length calculated as a sum of individual film widths. (c) Total peeling line (the sum of widths of all terminal elements) in fibrillar attachment systems of different animals as a function of their body mass (From Varenberg et al. 2010)

Furthermore, other advantages of such hairy adhesive systems have been proposed. For example, in a smooth, continuous adhesive contact, once a crack is initiated at the adhesive interface, the crack may easily propagate over the entire contact area until complete detachment occurs. By contrast, in a fibrillar system, the crack leads initially to the detachment of one seta, and the elastically stored energy in the seta is released and can no longer contribute to the propagation of the crack (Jagota and Bennison 2002; Hui et al. 2004; Chung and Chaudhury 2005; Tang and Hui 2005). This principle is known as crack trapping. Thus, the crack has to be reinitiated at each individual subcontact. In addition, fibrillar systems adapt better to uneven and rough surfaces (Persson 2003; Persson and Gorb 2003; Kim and Bhushan 2007; Filippov et al. 2011). Because each seta is virtually independent of other neighboring setae, a seta can contact the asperities and valleys of a rough surface without being mechanically influenced by neighboring setae (Fig. 9a). In contrast, in a smooth system, the region around the contact with a surface asperity can be prevented from forming contact (Fig. 9b). Moreover, the effective stiffness of a fibrillar adhesive system is strongly reduced compared with the stiffness of the bulk material of setae. Therefore, the fibrillar system is more compliant to rough surfaces (Persson 2003). Since these effects are based on fundamental physical principles and mostly related to the geometry of the structure, they must also hold for artificial surfaces with similar geometry.
Fig. 9

(a) Fibrillar and (b) smooth adhesive systems making contact with a rigid substrate with an asperity. Whereas in a fibrillar system, individual fibers can deform and follow surface irregularities without affecting neighboring setae (a), in smooth elastic pads, regions around the asperity can be prevented from forming contact (arrows; b) (From Heepe and Gorb 2014)

6 Contact Shape

Real biological adhesive contacts display a variety of shapes and only rarely resemble a hemisphere (Fig. 10). The influence of various contact shapes on the pull-off force for single contacts, as well as their scaling potential in contact arrays, was previously theoretically estimated (Spolenak et al. 2005) and experimentally demonstrated for artificial fibrillar adhesive systems (del Campo et al. 2007). It was concluded that non-spherical shapes, such as toroid, should lead to better attachment. In insects, spiders, and geckos, as shown in Fig. 7, the topmost hierarchical level of a seta that is responsible for the formation of intimate contact with the substrate resembles thin film-like or spatulae (Stork 1980b; Gorb 1998, 2000; Persson and Gorb 2003; Spolenak et al. 2005). Additionally, spatulae bear a gradient of thickness from the base to the tip of the spatula (fly, Gorb 1998; gecko, Persson and Gorb 2003; beetle, Eimüller et al. 2008) and a gradient in width as they become wider toward its free end. This geometrical property of setal tips can be observed in many animal species (Figs. 3 and 7). In contact, spatulae are aligned and orientated to the distal direction of the pad.
Fig. 10

Shapes of attachment devices in nature and their hypothetical evolutionary pathways (shown as arrows). (a) Bug Pyrrhocoris apterus, smooth pulvillus. (b) Grasshopper Tettigonia viridissima, surface of the attachment pad. (c) Fly Myathropa florea, unspecialized hairs on the leg. (d) Fly Calliphora vicina, seta of the pulvilli. (e) Ladybird beetle Harmonia axyridis, seta of the second tarsal segment. (f) Beetle Chrysolina fastuosa, seta of the second tarsal segment. (g) Male diving beetle Dytiscus marginalis, suction cups on the vertical side of the foreleg tarsi (Adapted from Spolenak et al. 2005). Band-like (tape-like, spatula-like) terminal contact elements (highlighted in gray) are most often observed in biological fibrillar adhesive systems capable of ceiling locomotion

Several hypotheses have been previously proposed to explain the functional importance of such a contact geometry: (1) enhancement of adaptability to the rough substrate (Persson and Gorb 2003), (2) contact formation by shear force rather than by normal load (Autumn et al. 2000), (3) increase of total peeling line due to using an array of multiple spatulae (Varenberg et al. 2010), and (4) contact breakage by peeling off (Gao et al. 2005).

It appeared that the role of highly flexible terminal spatula elements as compliant contacting surfaces is critical (Persson and Gorb 2003). Since the effective elastic modulus of thin plates is very small, even for relatively stiff materials such as keratin or arthropod cuticle, this geometry is of fundamental importance for adhesion on rough substrates (Persson and Gorb 2003), due to the low deformation energy stored in the material during intimate contact formation (Fig. 11).
Fig. 11

The role of the spatula-like terminal contact elements at the tips of adhesive setae in the adaptation to the surface profile (ac) and in the increasing of the total peeling line. (a) Contact of the spatula of the beetle Gastrophysa viridula with the microrough surface. (bc) Thick elastic material requires additional load to form adhesive contact (b), whereas adhesion interaction pulls the elastic thin film (even made of stiff material) into complete contact with the rough substrate surface (Adapted from Persson and Gorb 2003)

For adhesion activation, it is well known that the application of a normal load can enhance adhesion (Popov 2010). However, for hairy attachment systems, the adhesion force always remains smaller than the initially applied normal force. This would potentially be not enough to enable walking on the ceiling. Another possibility to activate or enhance adhesion forces is the application of a shear force. We have previously shown that an applied shear force to a particular direction of the spider’s spatulated setae results in an increase of real contact area (Niederegger and Gorb 2006; Filippov et al. 2011). Also, flies employ shear movements during contact formation by their attachment devices (Niederegger and Gorb 2003). Previous authors revealed strong shear dependence of measured pull-off force in the gecko attachment system and even called this effect by the somewhat misleading term frictional adhesion (Autumn et al. 2000, 2006), which can be simply explained by Kendall’s peeling model (Kendall 1975), when the tape is loaded/peeled off at very shallow angles to the substrate. In contrast, by peeling the tape off at very high angles, a very strong reduction in the adhesive force is obtained, which allows for a simple, quick, and energy-efficient detachment mechanism.

7 Slope and Hierarchy

The observed pull-off force of an adhesive structure may be defined by the difference between attractive forces arising due to, e.g., van der Waals or capillary interaction and the contact reaction forces, arising due to elastic deformation of the adhesive structure during contact deformation (Varenberg et al. 2011). In order to increase the pull-off force, either the attractive interactions have to increase, or the contact reaction forces have to decrease. The attractive forces, e.g., due to van der Waals interactions, reach a natural upper limit as soon as the adhesive structure and the contacting substrate form an intimate contact. In order to form intimate contact, especially to rough surfaces, adhesive structures have to be as soft as possible to enhance real contact area. This in turn, however, would increase the elastic deformations and thus the contact reaction force which would lead to a lower pull-off force. In light of the above, it is clear that there must be a trade-off for the adhesive structure between being soft enough, in order to form an intimate contact, and being stiff enough, to allow for the generation of a sufficiently high pull-off force. Solutions for this problem are either (a) in a hierarchical fibrillar design of the adhesive pad (Fig. 3d–f), (b) in a gradient material in nonhierarchical fibrillar structures (Fig. 12), or (c) in the tilted orientation of hairs relatively to the substrate (Fig. 13). In case of the gecko (see above), the complex hierarchical architecture of the adhesive pad made of relatively stiff β-keratin allows for a relatively low effective modulus (Persson 2003) while simultaneously avoiding setal condensation.
Fig. 12

Morphology and material composition of adhesive tarsal setae. Ventral part of the second adhesive pad of a foreleg of a female Coccinella septempunctata, lateral view. (a) Scanning electron micrograph. (b) CLSM maximum intensity projection showing an overlay of the four different autofluorescences indicating the material composition. The arrows indicate the dorsoventral material gradient in exemplary setae. S exemplary spatula-like seta, P exemplary seta with a pointed tip. Scale bars, 25 mm (From Peisker et al. 2013)

Fig. 13

Slope angle of adhesive setae in the tokay gecko Gekko gecko (a, b) (SEM) and in the fly Calliphora vicina (c) (semithin section, light microscopy). Arrows indicate distal direction of the pad (From Gorb 2011)

In geckos , there is a higher number of structural levels made of relatively stiff β-keratin (see above): lamella (the first lowermost level), seta (the second one), branching pattern of setulae (third and sometimes fourth level(s)), and spatulae (the uppermost one). Since many natural surfaces (stones, soil, tree bark, plants) have fractal roughness with several overlapping wavelengths, it is not enough to have adhesive pads optimized for one a particular wavelength of roughness. In order to optimize adhesion on a wide range of natural surfaces, biological fibrillar adhesives employed several hierarchical levels, each responsible for contact formation optimization for a particular range of wavelengths. In general, biological adhesive systems represent a kind of mirror structure of the natural fractal world.

Recently, numerous models were developed, in order to explain the role of the hierarchy in the functioning of biological adhesive pads (e.g., Kim and Bhushan 2007; Schargott 2009). While the hierarchical beam model with vertical beams shows the possibility of reducing the effective elastic modulus, the tilted beams are the key to obtaining very soft systems, even when the material employed has a high elastic modulus. In the model combining hierarchy and tilting, elastic and adhesive properties are furthermore enhanced (Schargott 2009). It is shown that when interacting with a rough stochastic surface, the attachment properties are improved with each additional hierarchical layer (Kim and Bhushan 2007; Schargott 2009).

Animals with fewer hierarchical levels have evolved different strategies for the same purpose. In the seven-spotted ladybird beetle (Coccinella septempunctata), a material gradient of tanned chitin at the setal base and the rubberlike resilin at the setal tip were recently found (Fig. 12; Peisker et al. 2013). Such a gradient in material properties similarly allows for an efficient adaptation to rough surfaces, due to the soft setal tip, while, at the same time, providing sufficient mechanical stability, due to stiffer base, to prevent clusterization and low contact reaction forces.

Tilted geometry of hairs is responsible for the bending mode of their deformation in contact rather than for the buckling one. It is clear that hairs are much stiffer in buckling than in bending. That is why tilted hair arrays have a much lower structural modulus of elasticity than a non-tilted one, and the adaptability to the surface profile of the tilted array is much higher. In addition, bending as a failure mode leads to lesser material fatigue than the buckling mode.

Additionally, asymmetrical shape of a single contact element in combination with the proper movements may provide the way to switchable adhesives, when contacts formed by fibers are activated and when the structure is sheared in the direction of the slope. The contact can be broken by peeling at high angles, when fibers are sheared in an opposite direction.

8 Adhesion Control

Animal locomotion involves simultaneous peeling of many spatulae, at the level of adhesive pads (Fig. 7), at the level of contralateral legs (Fig. 14a, b), and sometimes also at the level of contralateral toe pads within one foot (Fig. 14c). Thus, in climbing animals, the situation is more complex than in Kendall’s classical peeling model and resembles a hierarchical multiple peeling configuration (Pugno and Gorb 2009; Pugno 2011; Heepe et al. 2017a). On the macroscale, however, the peeling configuration of climbing animals may be reduced, for simplicity, to the peeling of two elastic tapes loaded at a common hinge (Fig. 14d). This double-peeling configuration has interesting adhesive properties, if compared to the classical single peeling. It exhibits a self-stabilized optimum peeling angle with a maximum in peeling force, i.e., the optimum configuration is reached irrespective of the initial peeling angle configuration of the system. Below the optimum angle, there is no delamination (peeling) but pure elastic deformation of the system. Above the optimum angle, stable delamination is observed. Figure 15 shows experimental results of the double-peeling configuration using an elastic adhesive tape (Heepe et al. 2017a).
Fig. 14

(a) A beetle Gastrophysa viridula in contact with a glass ceiling (lateral view from behind). The arrow indicates weight force W acting at the center of mass. (b) Fly Calliphora vicina in contact with a glass ceiling (view from above through the glass ceiling). Arrows indicate contralateral leg movement. (c) Foot of a gecko Gekko gecko in contact with a glass ceiling (view from above through the glass ceiling). Arrows indicate contralateral toe pad movement. (d) Simplified mechanical model of the ceiling situation (lateral view from behind, similar to (a). Two elastic tapes are in contact with a rigid ceiling and having a common hinge, where a load F is applied. The tapes make angles with respect to the substrate of α 1 and α 2 (From Heepe et al. 2017)

Fig. 15

(a) Schematic of the experimental setup. Principal double-peeling configuration: the tape (dark gray) is in contact with glass substrates (light gray) and loaded with a force F at the hinge in the middle of the tape. The tape makes initial peeling angles with the substrate of α 0. (b) Experimental results (open circles) of the double-peeling configuration using elastic adhesive tape. Experiments were started at initial peeling angles 0° and 90° as indicated by the arrows (Adapted from Heepe et al. 2017a)

When an animal is adhering to the ceiling, its legs tarsomeres are oriented toward the center of the body mass (Fig. 16a). In this orientation, setae are recruited by bending to their tilted direction, and spatulae are set under shear load. Under these conditions, setae are activated to their adhesive state. If five of the six insect legs are ablated, the animal is not able to adhere to the ceiling anymore, even if the average adhesive force of the single leg (measured for all six legs acting in concert and then normalized by the number of legs) should be sufficient to resist the body weight on the ceiling. However, with two intact legs, an animal can perfectly stay on the ceiling (Fig. 16b). With three remaining intact legs on one body side, an animal can reorient one leg to the other body side and stay on the ceiling (Fig. 16c). In the latter two cases, the adhesive system can be activated by shear force.
Fig. 16

(ac) Posture of the chrysomelid beetle Chrysolina fastuosa on the ceiling. (a) Intact beetles. (b) Two-legged beetles (four legs are removed). Arrows indicate orientation of leg tarsomeres. (c) Three-legged beetles (three legs on one body side are removed). Please note rearrangement of leg positions, in order to generate shear toward center of the body mass (arrows) (From Gorb 2011)

In light of the above results, the explanation of this phenomenon is rather simple. The situation of the single leg in contact can be simulated by a piece of sticky tape adhering to the ceiling and holding a certain mass. The peeling angle in such geometry would tend to be 90°, which according to Kendall’s model (Kendall 1975) generates a rather low peeling force. When two or multiple tapes are combined, the peeling angle will be generally lower than 90°, due to the self-stabilization effect of such geometry.

High-speed video recordings of a fly foot attaching to the substrate show that the pulvilli are pressed down to the surface and also pulled towards the body. Through this movement, the claws become spread apart (Fig. 17a, b). During such an action, setae and their spatulae will be activated, and the maximal force will be reached. In order to detach, four different movements may occur (Fig. 17cf) (Niederegger et al. 2001; Niederegger and Gorb 2003). (1) In shifting (or local peeling), the foot is shortly moved forward. This compresses the pulvilli, which in turn leads to a smaller contact area and thus to a reduction of attachment forces. Additionally, peeling occurred at the level of the spatulae. (2) In twisting, the leg is turned by up to 90° and pulled backward. This bends the setae and eventually detaches them from the surface. (3) In rotation (or global peeling), the foot is lifted from its back to the front, which causes the claws to be passively pressed to the surface. With this force, the adhesion is interrupted by peeling at the level of the whole pad. (4) In pulling, the foot is simply pulled backward until the attachment devices detach from the surface. This type of detachment possibly requires quite strong force, but it happens in some behavioral situations, especially when the insect is stressed. In geckos, attachment is activated by proximodistal rolling out of the toe, whereas detachment is provided by distoproximal peeling of it (Gao et al. 2005).
Fig. 17

Attachment and detachment movements of the fly adhesive organs (diagrams are based on the high-speed video recordings under binocular microscope). (a) Side view of attachment organs (pulvilli) in the fly Calliphora vicina (SEM). (b) Movement at attachment. (cf) Movements at detachment by using shifting (c), pulling (d), twisting (e), and rotation (c) (From Niederegger et al. 2001; Niederegger and Gorb 2003)

Observations of the gait pattern in flies walking on a horizontal surface revealed that three opposing legs were in the swing phase (moving), whereas the other three legs remained in the stance phase (motionless) (Fig. 18a). Does the gait pattern of the fly change on the wall and ceiling? Using high-speed camera video recordings of flies walking on a vertical surface, it was shown that their gait pattern is not different from the pattern on a horizontal surface. However, the fly walking on the ceiling moved only two legs at once and four remained in the stance phase (Niederegger et al. 2001; Gorb 2001, 2005) (Fig. 18b). This result led us to assume that the gait pattern may contribute to the fly’s ability to adhere dynamically on the ceiling, in providing an optimal relationship between the body weight and the supporting contact area.
Fig. 18

Gait patterns of insects on glass ceiling. (a, b) Gait diagram of the house fly, Musca domestica, on the floor (a) and ceiling (b) (From Niederegger et al. 2001; Gorb 2001, 2005). (c) Relationship between the safety factor (attachment force divided by the body weight) and the gait pattern on the ceiling in different insects. Insets show feet (black dots) that are typically in contact during the walk on smooth ceiling (From Gorb 2011)

Experiments with insect species that have different safety factors (attachment force divided by the body weight) show that insects with a safety factor above 10 can employ tripod gait similar to one observed during locomotion on the floor. Insects with a safety factor in the range of 4–5 change their gait compared to that reported above for the fly. Insects with a safety factor lower than 3 change their gait to that, where only one leg is in the swing phase and the other five remain in the stance phase (Fig. 18c). These results show that dynamical adhesion in insects may also strongly rely on a multiple peeling configuration, especially in ceiling locomotion.

Thus, it is plausible to assume that biological adhesive systems try to actively use changes in their configuration of their tape-like contact geometry, to control and/or maintain adhesion. To securely stay on the ceiling, animals tend to keep their macroscopic peeling angle below the optimum. In this regime, no peeling occurs. Interestingly, in flies clinging to a glass ceiling, it was observed that their feet were in constant slow motion toward the body center of mass (Wigglesworth 1987), potentially due to the tarsal secretions produced in insect adhesive systems (Gorb 2001b). After a certain sliding motion of the feet, they were quickly extended and reattached, thereby maintaining a position with a low macroscopic peeling angle. Quick and easy detachment may be achieved by a simple active change of the macroscopic peeling angle above the optimum one by, e.g., proximodistal peeling in the case of flies (Niederegger et al. 2002) and distoproximal peeling or digital hyperextension in the case of geckos (Russel 1975). This may be possible, since their available contact area is restricted to the pad area and, thus, only a short peeling distance is necessary before complete detachment of a pad or a foot occurs.

9 Environmental Conditions Affecting Animal Adhesion

All natural surfaces have surface roughness on many different length scales (Persson 2014) which may strongly reduce attachment of animals (e.g., Gorb 2001; Gorb and Gorb 2002; Peressadko and Gorb 2004b; Huber et al. 2007; Voigt et al. 2008; Wolff and Gorb 2012). The influence of surface roughness on insect attachment has been proven experimentally in several studies (Gorb 2001; Peressadko and Gorb 2004b; Voigt et al. 2008; Bullock and Federle 2011). There seems to be a common trend that insects generate much higher forces on either smooth or rough surfaces with an asperity size exceeding 3.0 μm than on those with the roughness ranging from 0.3 to 3.0 μm (Fig. 19). This effect has been explained by the specific geometry of spatula-like terminal elements of insect tenent setae that are able to generate sufficient contact, if the surface irregularities are sufficiently large. Worst attachment has been observed on substrates with a roughness of 0.3 and 1.0 μm (Fig. 19). In this case, the spatula-like terminal elements cannot follow the surface profiles with these small asperities, and thus, the area of real contact between these substrates and the tips of insect setae is very small. Since adhesion force depends on the area of real contact, insects were not able to attach successfully to surfaces with such a microroughness.
Fig. 19

Role of the substrate roughness (asperity diameter) in the attachment of biological fibrillar adhesives. (a) Attachment forces of chrysomelid beetles Gastrophysa viridula measured on the horizontal surface of the drum of the centrifugal force tester on substrates with different roughness. (b) Surface of the substrate in SEM and measured with the profilometer (From Peressadko and Gorb 2004b)

Interesting examples of natural anti-adhesive surfaces are well known from many plants, which are covered with microscopic wax crystals of different shapes, chemistry, and mechanical properties. To explain the anti-adhesive properties of these plant substrates, four hypotheses were previously proposed (Gorb and Gorb 2002). (i) Wax crystals cause microroughness, which considerably decreases the real contact area between the substrate and setal tips of adhesive pads (roughness hypothesis); see above. (ii) Wax crystals are easily detachable structures that contaminate pads (contamination hypothesis). (iii) Structured wax coverage may absorb the fluid from the setal surface (fluid absorption hypothesis). (iv) Insect pad secretion may dissolve wax crystals (wax-dissolving hypothesis). This would result in the appearance of a thick layer of fluid, making the substrate slippery. Recently, only the first three hypotheses were tested.

Contamination of insect pads by plant wax crystals has been demonstrated for several insects and in a series of plant species (e.g., Gaume et al. 2004; Gorb and Gorb 2006). It has been found that plants differ essentially in their contaminating effects on insect pads (Gorb and Gorb 2006). The degree of contamination depends on the micromorphology of waxes (Borodich et al. 2010). The analysis of the relationship between the contamination ability and geometrical parameters of wax crystals has shown that the contamination is related to both the largest dimension and the aspect ratio of crystals (Borodich et al. 2010).

The fluid absorption hypothesis was recently tested in an experimental study, where nanoporous substrates with the same pore diameter but different porosity (area of voids in a material surface, normalized over the total area) were used (Gorb et al. 2010). According to this hypothesis, absorption of the insect pad fluid by the porous substrate results in a reduction in the fluid thickness between the terminal plates of the insect pads and the substrate, and this leads to a reduction of capillary interaction in the contact area. Traction force experiments performed on tethered ladybird beetles walking on different porous substrates showed that forces were significantly reduced. The reduction in insect attachment on nanoporous surfaces may be explained by possible absorption of the secretion fluid from insect adhesive pads by porous media and/or the effect of surface roughness. The wax-dissolving hypothesis has not been experimentally tested yet.

A rather long-standing question in animal attachment is which substrate property is most important for the attachment ability: surface roughness or surface chemistry? Since the surface chemistry (here in terms of surface energy) affects the strength of either van der Waals or capillary interaction, substrates with low surface energy are expected to reduce the overall attachment ability. In a recent experiment, traction forces of ladybird beetles Coccinella septempunctata were systematically measured on eight types of substrates, each with different chemical and topographical properties (England et al. 2016). The results clearly showed that surface roughness rather than surface chemistry essentially affected insect adhesion. Surface chemistry had no significant effect on the attachment ability of the beetles (England et al. 2016).

So far, however, the attachment ability of insects and also that of spiders and geckos has been tested on rigid substrates only, whereas the natural habitats of climbing animals may provide a variety of substrate stiffness ranging from rigid rock surfaces to soft, biofilm-covered substrates. Friction force measurements, using a centrifugal force tester, with male and female beetles Coccinella septempunctata on smooth silicone elastomer substrates with different stiffness between 2 and 0.3 MPa revealed an overall decrease in attachment ability if compared to a rigid substrate (Heepe et al. 2017b). Within the range of measured stiffness, female’s attachment ability was not affected, whereas male’s decreased with decreasing stiffness. This sexual dimorphism in attachment ability is explained by the presence of a specialized, discoidal seta type in males, which is not present in females (Heepe et al. 2017b). Substrate properties are not the only environmental factors shown to influence animal adhesion. Also the ambient humidity affects the attachment ability, as it was shown in the dry adhesive pads of geckos (Huber et al. 2005a; Niewiarowski et al. 2008; Puthoff et al. 2010; Prowse et al. 2011) and spiders (Wolff and Gorb 2011) as well as in the wet adhesive pads of beetles (Heepe et al. 2016). In all animals, reduced attachment ability was observed for very low and very high relative humidities, whereas maximum attachment ability was found for intermediate humidities (Heepe et al. 2016). This is particularly interesting since both types of adhesive systems (wet and dry) are supposed to be based on different physical interactions (capillarity versus van der Waals forces).

10 Biomimetic Implications

As mentioned above, fibrillar adhesive systems appeared several times in animal evolution and at least three times independently even in insect evolution. This fact may indicate that design principles of biological fibrillar adhesives must have an advantage for adhesion enhancement not only in biological systems but also in artificial surfaces having similar geometry. Geometrical effects discussed above, such as multiple individual contacts, high aspect ratio of single contact structures, peeling spatula-like tips of single contact elements, are responsible not only for generation of a strong pull-off force in such devices but also for other interesting features, such as adhesion reversibility, contamination reduction, etc. (Fig. 20). The physical background of these effects were intensively discussed theoretically in several publications (for early original work, see, e.g., Jagota and Bennison 2002; Arzt et al. 2003; Persson 2003; Persson and Gorb 2003; Chung and Chaudhury 2005; Gao et al. 2005; and for current reviews, Federle 2006; Autumn 2007; Kampermann et al. 2010; Gorb 2011; Jagota and Hui 2011). For fibrillar biological systems, the following key functional properties can be defined (Autumn et al. 2007; Creton and Gorb 2007).
  1. 1.

    Anisotropic attachment: Attachment force variable depending on the setal-spatula orientation with respect to the substrate, normal load, and parallel drag.

     
  2. 2.

    High adhesion coefficient: Ratio of preload to pull-off force, which represents the strength of adhesion as a function of the compressive load.

     
  3. 3.

    Low detachment force: Animals detach their feet in a few milliseconds by different kinds of movement, which lead to peeling of adhesive structures at different levels.

     
  4. 4.

    Universality of adhesion: Van der Waals-based interaction and oil-based capillary interaction with the substrate depend basically on geometry of features (fibrillar shape, spatulae, fluid thickness, etc.) and are less dependent on the substrate chemistry.

     
  5. 5.

    Self-cleaning: The feet of geckos are resistant to the contamination by particles corresponding in size to typical environmental dirt particles (diameter 5–100 μm). In insects, secreted fluid may additionally contribute to rinsing of dirt particles. Biological fibrillar adhesive systems possess an anti-contaminating property.

     
  6. 6.

    Anti-self-adhesion: Hierarchical fibrillar structure avoids the self-adhesion of individual structural elements.

     
  7. 7.
    Nonsticky default state: Most of the fibrillar structures with an exception of mushroom-shaped setae are nonsticky by default, because only a very small contact fraction is possible without deforming the setal array.
    Fig. 20

    Some functional principles (FEATURE) at which biological reversible and biological adhesive systems operate. In the middle of the diagram, the functions (FUNCTION) and their relationship to the features are depicted. The resulting effect that is required for optimization is shown at the right-hand side (arrows indicate enhancement/reduction of the function). Simultaneous implementation of all these features in one artificial system is desirable but hardly possible. However, one principle or a combination of few of them can be implemented depending on particular requirements for material or system (From Gorb et al. 2007b)

     
Based on the inspiration from biology and using contact theory as a guideline, artificial surfaces were developed with enhanced pull-off forces in contact with the flat surface, if compared to the flat control. These materials have been produced using various micro- and nanofabrication techniques ranging from laser technology and carbon nanotube packaging to various lithography techniques (for early original work, see, e.g., Geim et al. 2003; Sitti and Fearing 2003; Peressadko and Gorb 2004a; Northen and Turner 2005; Yurdumakan et al. 2005; and for current reviews, e.g., Greiner et al. 2009; Sameoto and Menon 2010; Kwak et al. 2011) (Fig. 21). Independently on the pull-off forces achieved by the surface patterning, these materials are strongly limited in the patterned area. Usually, the overall patterned area was in the best case restricted to few square centimeters, which makes their use for industrial applications rather difficult. Also most bioinspired fibrillar adhesives are just based on the fibers with flat punches at their tips or in most elaborate cases sloped punches (Autumn et al. 2007), without implementation of proper terminal elements in the form of spatula or mushroom, as we know them from the majority of biological systems including insects, spiders, and geckos. So far, the best results of mimicking fibrillar adhesive systems have been achieved with mushroomlike surface microstructures (for early original work, see, e.g., Daltorio et al. 2005; Kim and Sitti 2006; Gorb et al. 2007a; Davies et al. 2009; for a current review, see Heepe and Gorb 2014). Some of these developments may be produced in large-scale industrial processes in the form of square meters large foils (Gottlieb Binder and Co 2017) (Fig. 22). Interestingly, such microstructures can be found in attachment pads of male beetles from the family Chrysomelidae. Although both sexes possess adhesive hairs on their tarsi, only males bear hairs with such extreme specialization for adhesion on the smooth surface and most likely to attach to female’s covering wings during pairing (Stork 1980b; Voigt et al. 2008). It has been previously reported that males of the Colorado potato beetle Leptinotarsa decemlineata generate such a strong adhesion on the smooth clean glass that they are not able to break off the contact and that is why they have a hard time walking on this surface (Pelletier and Smilowitz 1987). The hairs responsible for this effect have broad flattened tips and narrowed flexible region below the tips. These features, as well as distribution patterns of pillars, were implemented in the design of the patterned polymer structure described here.
Fig. 21

Bioinspired fibrillar adhesives of different dimensions. (a, b) Metallic nanowhiskers. (c, d) Hierarchically branching fiber arrays made of epoxy resin. (e, f) Silicone molds of laser-patterned metal surface. (g, h) Carbon nanotubes. (ad, g, h) Original micrographs ((ad, g, h) From Gorb 2010. (e, f) From Peressadko and Gorb 2004a)

Fig. 22

Patterned insect-inspired polivinylsiloxane surface. (a) Single structures are distributed on the surface according to the hexagonal pattern, in order to reach the highest packaging degree of single pillars (above aspect, SEM image). (b) White light interferometer image of a single pillar head demonstrates almost flat shape of the contacting surface. (c) Side aspect of the pillar array. (df) Behavior of structured PVS surfaces in contact with the glass surface (SEM images). Black arrowhead shows a dust particle in contact (From Gorb et al. 2007b)

The adhesive properties of the industrial micropatterned adhesive foil were characterized using a variety of measurement techniques and compared with those of the flat foil made of the same polymer (Daltorio et al. 2005; Gorb et al. 2007a; Varenberg and Gorb 2008a, b, c; Heepe et al. 2011, 2012, 2013, 2014a, b, 2017a; Kovalev et al. 2012; Kizilkan et al. 2013, 2017; Kasem and Varenberg 2013; Dening et al. 2014; Breckwoldt et al. 2015). The foil with the microstructure pattern demonstrates considerably higher pull-off force per unit real contact area and per unit apparent contact area as well. It is also less sensitive to contamination by dust particles, and after being contaminated and washed with soap and water, the adhesive properties can be completely recovered. The foil represents an industrial dry adhesive based on the combination of several principles previously found in biological attachment devices of insects, spiders, and geckos.

This material is a promising candidate for the application in dynamical adhesive systems, such as robot soles adapted for locomotion. Robots that could climb smooth and complex inclined terrains, like insects and lizards, would have many applications such as exploration, inspection, or cleaning. Walking machines usually use suckers to hold onto vertical surfaces and under a surface. A primary disadvantage of this attachment principle is large energy consumption for vacuum maintenance. The novel biologically inspired materials may enable future robots to walk on smooth surfaces regardless of the direction of gravity. Mini-Whegs™, a small robot (120 g) that uses four-wheel legs for locomotion, was recently converted to a wall-walking robot with compliant, adhesive feet (Daltorio et al. 2005). The robot is capable of ascending vertical smooth glass surfaces using a micropatterned adhesive (Fig. 23a). A new version of this robot (about 22 g) is even able to transverse from the floor to the ceiling without detaching from the substrate (Fig. 23b). Another demonstration of adhesion capability of such material is shown in Fig. 23c, d. A PMMA plate, 20 × 20 cm, covered by the foil is sufficient to support the weight of a man attached to the glass ceiling (Fig. 23c). Using custom-built gloves for hands and feet, the material, in principle, allows climbing a vertical glass wall (Fig. 23d).
Fig. 23

(a) Mini-Whegs™ on vertical glass with a microstructured adhesive tape (From Daltorio et al. 2005). (b) Inverted Mini-Whegs demonstrating internal transitions from floor to wall to ceiling (From Breckwoldt et al. 2015). (c) Photograph of a man attached to the glass ceiling by a 20 × 20 cm PMMA plate covered by microstructured adhesive tape (see SEM image in the inset) (original). (d) Photograph of a man attached to a vertical glass wall by custom-built gloves for hands and feet covered with the microstructured adhesive tape (original)

Bioinspired fibrillar materials can be additionally applied to the design of microgripper mechanisms with the ability to reversibly adhere and to adapt to a variety of surface profiles and for any kind of reversible adhesive tapes.

11 Conclusions

  1. 1.

    Real biological attachment systems usually rely on the combination of different functional principles based on elaborate micro- and nanostructures.

     
  2. 2.

    Attachment systems in biology can be subdivided according to their structure and basic physical forces responsible for enhancement of contact forces.

     
  3. 3.

    Reversible attachment devices used for locomotion may be hairy and smooth. Hairy systems consist of fine microstructures, whereas smooth systems are composed of materials with unusual inner structure. Due to the flexibility of the material of the attachment pads or fine surface structures, both mechanisms can maximize the possible contact area with a wide range of substrate profiles.

     
  4. 4.

    Recent phylogenetic analyses have shown that similar functional solutions for attachment have evolved several times independently in the evolutionary history of animals (e.g., geckos, anoles, spiders, beetles, flies, etc.).

     
  5. 5.

    In hairy systems, the density of single contact elements usually increases with increasing body weight of the animal group. From the scaling analysis, it has been previously suggested that animal lineages relying on dry adhesion (lizards, spiders) possess a much higher density of terminal contact elements compared to systems using the wet adhesive mechanism (insects).

     
  6. 6.

    Lizards’ and spiders’ attachment systems are mainly based on van der Waals forces, but also wetting phenomena caused by water absorbed on the surface have an effect on the attachment ability. In insects, mainly attractive capillary and viscous forces mediated by the pad secretion are the basic physical mechanism in their adhesion.

     
  7. 7.

    The effective elastic modulus of the fiber arrays is very small, which is of fundamental importance for proper contact formation and adhesion on smooth and rough substrates.

     
  8. 8.

    Hierarchical organization of surface features in attachment pads may enhance adaptability to real surfaces, which often have fractal roughness.

     
  9. 9.

    Asymmetrical shape of single contact element (tilted position relative to the support) in combination with proper movements may provide a way to switchable adhesives.

     
  10. 10.

    Hairy pads show a clearly cut minimum of adhesion at certain ranges of substrate roughness. Such a critical range of roughness depends on the relationship between the diameter of single contact elements of the pad and the length scale of the roughness.

     
  11. 11.

    During their evolution, plants have developed structures to prevent adhesion of insects. To explain anti-adhesive properties of plants, structured with crystalline waxes, four hypotheses were proposed: (1) roughness hypothesis, (2) contamination hypothesis, (3) wax-dissolving hypothesis, and (4) fluid absorption hypothesis.

     
  12. 12.

    Since many functional effects found in biological systems are based on fundamental physical principles which are mostly related to the geometry of the structure, they must hold also for artificial surfaces with similar geometry.

     

References

  1. Alibardi L (1997) Ultrastructural and autoradiographic analysis of setae development in the embryonic pad lamellae of the lizard Anolis lineatopus. Ann Sci Nat Zool Biol Anim 18:51Google Scholar
  2. Arzt E, Gorb SN, Spolenak R (2003) From micro to nano contacts in biological attachment devices. Proc Natl Acad Sci U S A 100:10603CrossRefGoogle Scholar
  3. Autumn K, Liang YA, Hsieh ST, Zesch W, Chan WP, Kenny TW, Fearing R (2000) Adhesion force measurements on single gecko setae. Nature 405:681CrossRefGoogle Scholar
  4. Autumn K, Sitti M, Liang YA, Peattie AM, Hansen M (2002) Evidence for van der Waals adhesion in gecko setae. Proc Natl Acad Sci U S A 99:12252CrossRefGoogle Scholar
  5. Autumn K, Dittmore A, Santos D, Spenko M, Cutkosky M (2006) Frictional adhesion: a new angle on gecko attachment. J Exp Biol 209:3569CrossRefGoogle Scholar
  6. Autumn K, Gravish N, Wilkinson M, Santos D, Spenko M, Cutkosky M (2007) Frictional adhesion of natural and synthetic gecko setal arrays. In: Proceedings of 30th annual meeting adhesion society, Inc, The Adhesion Society, Blacksburg, VAGoogle Scholar
  7. Barnes WJP (2006) Whole animal measurements of shear and adhesive forces in adult tree frogs: insights into underlying mechanisms of adhesion obtained from studying the effects of size and scale. J Comp Physiol A 192:1179CrossRefGoogle Scholar
  8. Bauchhenss E (1979) Die Pulvillen von Calliphora erythrocephala (Diptera, Brachycera) als Adhäsionsorgane. Zoomorphologie 93:99CrossRefGoogle Scholar
  9. Betz O (2010) Adhesive exocrine glands in insects: morphology, ultrastructure, and adhesive secretion. In: Byern J, Grunwald I (eds) Biological adhesive systems. From nature to technical and medical application. Springer, Vienna, pp 111–152Google Scholar
  10. Beutel RG, Gorb SN (2001) Ultrastructure of attachment specializations of hexapods (Arthropoda): evolutionary patterns inferred from a revised ordinal phylogeny. J Zool Syst Evol Res 39:177CrossRefGoogle Scholar
  11. Beutel RG, Gorb SN (2006) A revised interpretation of the evolution of attachment structures in Hexapoda with special emphasis on Mantophasmatodea. Arthrop Syst Phylogeny 64(1):3–25Google Scholar
  12. Borodich FM, Gorb EV, Gorb SN (2010) Fracture behaviour of plant epicuticular wax crystals and its role in preventing insect attachment: a theoretical approach. Appl Phys A Mater Sci Process 100:63CrossRefGoogle Scholar
  13. Breckwoldt WA, Daltorio K, Heepe L, Horchler AD, Gorb SN, Quinn R (2015) Walking inverted on ceilings with wheel-legs and micro-structured adhesives. In: Intelligent robots and systems (IROS), IEEE/RSJ international conference on. IEEE, Hamburg, Germany, pp 3308–3313Google Scholar
  14. Bullock JMR, Federle W (2011) The effect of surface roughness on claw and adhesive hair performance in the dock beetle Gastrophysa viridula. Insect Sci 18:298CrossRefGoogle Scholar
  15. del Campo A, Greiner C, Arzt E (2007) Contact shape controls adhesion of bioinspired fibrillar surfaces. Langmuir 23:10235CrossRefGoogle Scholar
  16. Chung JY, Chaudhury MK (2005) Roles of discontinuities in bio-inspired adhesive pads. J R Soc Interface 2:55CrossRefGoogle Scholar
  17. Creton C, Gorb SN (2007) Sticky feet: from animals to materials. MRS Bull 32:466CrossRefGoogle Scholar
  18. Daltorio KA, Gorb SN, Peressadko A, Horchler AD, Ritzmann RE, Quinn RD (2005) A robot that climbs walls using micro-structured polymer feet. In: Proceedings of international conference on climbing and walking robots CLAWAR, London, UK, pp 131–138Google Scholar
  19. Davies J, Haq S, Hawke T, Sargent JP (2009) A practical approach to the development of a synthetic Gecko tape. Int J Adhes Adhes 29:380CrossRefGoogle Scholar
  20. Dening K, Heepe L, Afferrante L, Carbone G, Gorb SN (2014) Adhesion control by inflation: implications from biology to artificial attachment device. Appl Phys A Mater Sci Process 116:567CrossRefGoogle Scholar
  21. Edwards JS, Tarkanian M (1970) The adhesive pads of Heteroptera: a re-examination. Proc Roy Ent Soc Lond A 45:1Google Scholar
  22. Eimüller T, Guttmann P, Gorb SN (2008) Terminal contact elements of insect attachment devices studied by transmission X-ray microscopy. J Exp Biol 211:1958CrossRefGoogle Scholar
  23. Eisner T, Aneshansley DJ (2000) Defense by foot adhesion in a beetle (Hemisphaerota cyanea). Proc Natl Acad Sci U S A 97:6568CrossRefGoogle Scholar
  24. England MW, Sato T, Yagihashi M, Hozumi A, Gorb SN, Gorb EV (2016) Surface roughness rather than surface chemistry essentially affects insect adhesion. Beistein J Nanotechnol 7:1471CrossRefGoogle Scholar
  25. Federle W (2006) Why are so many adhesive pads hairy? J Exp Biol 209:2611CrossRefGoogle Scholar
  26. Federle W, Riehle M, Curtis ASG, Full RJ (2002) An integrative study of insect adhesion: Mechanics and wet adhesion of pretarsal pads in ants. Integr Comp Biol 42:1100CrossRefGoogle Scholar
  27. Filippov AE, Popov VL, Gorb SN (2011) Shear induced adhesion: Contact mechanics of biological spatula-like attachment devices. J Thero Biol 276:126MathSciNetCrossRefGoogle Scholar
  28. Gao H, Wang X, Yao H, Gorb SN, Arzt E (2005) Mechanics of hierarchical adhesion structures of geckos. Mech Mater 37:275CrossRefGoogle Scholar
  29. Gaume L, Perret P, Gorb E, Gorb S, Labat J-J, Rowe N (2004) How do plant waxes cause flies to slide? Experimental tests of wax-based trapping mechanisms in three pitfall carnivorous plants. Arth Struct Dev 33:103CrossRefGoogle Scholar
  30. Geim AK, Dubonos SV, Grigorieva IV, Novoselov KS, Zhukov AA (2003) Microfabricated adhesive mimicking gecko foot-hair. Nat Mater 2:461CrossRefGoogle Scholar
  31. Geiselhardt SF, Geiselhardt S, Peschke K (2009) Comparison of tarsal and cuticular chemistry in the leaf beetle Gastrophysa viridula (Coleoptera: Chrysomelidae) and an evaluation of solid-phase microextraction and solvent extraction techniques. Chemoecology 19:185CrossRefGoogle Scholar
  32. Geiselhardt SF, Federle W, Prüm B, Geiselhardt S, Lamm S, Peschke K (2010) Impact of chemical manipulation of tarsal liquids on attachment in the Colorado potato beetle, Leptinotarsa decemlineata. J Insect Physiol 56:398CrossRefGoogle Scholar
  33. Gladun D, Gorb SN, Frantsevich LI (2009) Alternative tasks of the insect arolium with special reference to hymenoptera. In: Gorb SN (ed) Functional surfaces in biology – adhesion related phenomena, vol 2. Springer, Dordrecht/Heidelberg/London/New York, pp 67–103CrossRefGoogle Scholar
  34. Gorb SN (1998) The design of the fly adhesive pad: distal tenent setae are adapted to the delivery of an adhesive secretion. Proc Roy Soc Lond B 265:747CrossRefGoogle Scholar
  35. Gorb SN (2000) Biological microtribology: anisotropy in frictional forces of orthopteran attachment pads reflects the ultrastructure of a highly deformable material. Proc Roy Soc Lond B 267:1239CrossRefGoogle Scholar
  36. Gorb SN (2001) Attachment devices of insect cuticle. Springer, New YorkGoogle Scholar
  37. Gorb SN (2005) Uncovering insect stickiness: structure and properties of hairy attachment devices. Amer Ent 51:31CrossRefGoogle Scholar
  38. Gorb SN (2007) Smooth Attachment Devices in Insects: Functional Morphology and Biomechanics. Adv In Insect Phys 34:81CrossRefGoogle Scholar
  39. Gorb SN (2009) Adhesion in nature. In: Brockmann W, Geiß PL, Klingen J, Schröder B (eds) Adhesive bonding – materials, applications and technology. Wiley-VCH, Weinheim, pp 346–356Google Scholar
  40. Gorb SN (2010) Biological and biologically inspired attachment systems. In: Bhushan B (ed) Springer handbook of nanotechnology. Springer Verlag, Berlin, pp 1525–1551CrossRefGoogle Scholar
  41. Gorb SN (2011) Biological fibrillar adhesives: functional principles and biomimetic applications. In: da Silva LFM, Öchsner A, Adams RD (eds) Handbook of adhesion technology, pp 1409–1436. doi: 10.1007/978-3-642-01169-6_54 CrossRefGoogle Scholar
  42. Gorb SN, Beutel RG (2001) Evolution of locomotory attachment pads of hexapods. Naturwissenschaften 88:530CrossRefGoogle Scholar
  43. Gorb EV, Gorb SN (2002) Attachment ability of the beetle Chrysolina fastuosa on various plant surfaces. Entomol Exp Appl 105:13CrossRefGoogle Scholar
  44. Gorb EV, Gorb SN (2006) Do plant waxes make insect attachment structures dirty? Experimental evidence for the contamination hypothesis. In: Herrel A, Speck T, Rowe N (eds) Ecology and biomechanics: a mechanical approach to the ecology of animals and plants. Taylor & Francis, Boca Raton, pp 147–162CrossRefGoogle Scholar
  45. Gorb SN, Varenberg M (2007) Mushroom-shaped geometry of contact elements in biological adhesive systems. J Adhes Sci Technol 21:1175CrossRefGoogle Scholar
  46. Gorb SN, Varenberg M, Peressadko A, Tuma J (2007a) Biomimetic mushroom-shaped fibrillar adhesive microstructure. J R Soc Interface 4:271CrossRefGoogle Scholar
  47. Gorb SN, Sinha M, Peressadko A, Daltorio KA, Quinn RD (2007b) Insects did it first: a micropatterned adhesive tape for robotic applications. Bioinspir Biomim 2:S117CrossRefGoogle Scholar
  48. Gorb EV, Hosoda N, Miksch C, Gorb SN (2010) Slippery pores: anti-adhesive effect of nanoporous substrates on the beetle attachment system. J R Soc Interface 7:1571CrossRefGoogle Scholar
  49. Gottlieb Binder GmbH & Co KG (2017) http://www.binder.de/en/products/geckonanoplast/
  50. Greiner C, Arzt E, del Campo A (2009) Hierarchical Gecko - Like Adhesives. Adv Mater 21:479CrossRefGoogle Scholar
  51. Heepe L, Gorb SN (2014) Biologically inspired mushroom-shaped adhesive microstructures. Annu Rev Mater Res 44:173CrossRefGoogle Scholar
  52. Heepe L, Varenberg M, Itovich Y, Gorb SN (2011) Suction component in adhesion of mushroom-shaped microstructure. J R Soc Interface 8:585CrossRefGoogle Scholar
  53. Heepe L, Kovalev AE, Varenberg M, Tuma J, Gorb SN (2012) First mushroom-shaped adhesive microstructure: A review. Thero Appl Mech Lett 2:014008Google Scholar
  54. Heepe L, Kovalev AE, Filippov AE, Gorb SN (2013) Adhesion failure at 180 000 frames per second: direct observation of the detachment process of a mushroom-shaped adhesive. Phys Rev Lett 111:104301CrossRefGoogle Scholar
  55. Heepe L, Carbone G, Pierro E, Kovalev AE, Gorb SN (2014a) Adhesion tilt-tolerance in bio-inspired mushroom-shaped adhesive microstructure. Appl Phys Lett 104:011906CrossRefGoogle Scholar
  56. Heepe L, Kovalev AE, Gorb SN (2014b) Direct observation of microcavitation in underwater adhesion of mushroom-shaped adhesive microstructure. Beilstein J Nanotechnol 5:903CrossRefGoogle Scholar
  57. Heepe L, Wolff JO, Gorb SN (2016) Influence of ambient humidity on the attachment ability of ladybird beetles (Coccinella septempunctata). Beilstein J Nanotechnol 7:1332CrossRefGoogle Scholar
  58. Heepe L, Raguseo S, Gorb SN (2017a) An experimental study of double-peeling mechanism inspired by biological adhesive systems. Appl Phys A Mater Sci Process 123:124CrossRefGoogle Scholar
  59. Heepe L, Petersen DS, Tölle L, Wolff JO, Gorb SN (2017b) Sexual dimorphism in the attachment ability of the ladybird beetle Coccinella septempunctata on soft substrates. Appl Phys A Mater Sci Process 123:34CrossRefGoogle Scholar
  60. Hiller U (1968) Untersuchungen zum Feinbau und zur Funktion der Haftborsten von Reptilien. Z Morphol Tiere 62:307CrossRefGoogle Scholar
  61. Homann H (1957) Haften Spinnen an einer Wasserhaut? Naturwissenschaften 44:318CrossRefGoogle Scholar
  62. Huber G, Gorb SN, Spolenak R, Arzt E (2005a) Resolving the nanoscale adhesion of individual gecko spatulae by atomic force microscopy. Biol Lett 1:2CrossRefGoogle Scholar
  63. Huber G, Mantz H, Spolenak R, Mecke K, Jacobs K, Gorb SN, Arzt E (2005b) Evidence for capillarity contributions to gecko adhesion from single spatula nanomechanical measurements. Proc Natl Acad Sci U S A 102:16293CrossRefGoogle Scholar
  64. Hui CY, Glassmaker NJ, Tang T, Jagota A (2004) Design of biomimetic fibrillar interfaces: 2. Mechanics of enhanced adhesion. J R Soc Interface 1:35CrossRefGoogle Scholar
  65. Ishii S (1987) Adhesion of a Leaf Feeding Ladybird Epilachna vigintioctomaculta (Coleoptera: Coccinellidae) on a Virtically Smooth Surface. Appl Entomol Zool 22:222CrossRefGoogle Scholar
  66. Israelachvili JN (1992) Intermolecular and surface forces: With Applications to Colloidal and Biological Systems, 2nd edn. Academic, LondonGoogle Scholar
  67. Jagota A, Bennison SJ (2002) Mechanics of adhesion through a fibrillar microstructure. Integr Comp Biol 42:1140CrossRefGoogle Scholar
  68. Jagota A, Hui C-Y (2011) Adhesion, friction, and compliance of bio-mimetic and bio-inspired structured interfaces. Mater Sci Eng R Rep 72:253Google Scholar
  69. Johnson KL, Kendall K, Roberts AD (1971) Surface energy and the contact of elastic solids. Proc R Soc Lond A 324:301CrossRefGoogle Scholar
  70. Kampermann M, Kroner E, del Campo A, McMeeking RM, Arzt E (2010) Functional Adhesive Surfaces with “Gecko” Effect: The Concept of Contact Splitting. Adv Eng Mater 12:335CrossRefGoogle Scholar
  71. Kasem H, Varenberg M (2013) Effect of counterface roughness on adhesion of mushroom-shaped microstructure. J R Soc Interface 10:20130620CrossRefGoogle Scholar
  72. Kendall K (1975) Thin-film peeling-the elastic term. J Phys D Appl Phys 8:1449CrossRefGoogle Scholar
  73. Kesel AB, Martin A, Seidl T (2003) Adhesion measurements on the attachment devices of the jumping spider Evarcha arcuata. J Exp Biol 206:2733CrossRefGoogle Scholar
  74. Kim TW, Bhushan B (2007) Adhesion analysis of multi-level hierarchical attachment system contacting with a rough surface. J Adhes Sci Technol 21:1Google Scholar
  75. Kim S, Sitti M (2006) Biologically inspired polymer microfibers with spatulate tips as repeatable fibrillar adhesives. Appl Phys Lett 89:26911Google Scholar
  76. Kizilkan E, Heepe L, Gorb SN (2013) Underwater adhesion of mushroom-shaped adhesive microstructure: an air-entrapment effect. In: Biological and Biomimetic Adhesives: Challenges and Opportunities. RCS, Cambridge, pp 65–71Google Scholar
  77. Kizilkan E, Strueben J, Staubitz A, Gorb SN (2017) Bioinspired photocontrollable microstructured transport device. Sci Robotics 2:eaak9454CrossRefGoogle Scholar
  78. Kosaki A, Yamaoka R (1996) Chemical composition of footprints and cuticula lipids of three species of lady beetles. Jpn J Appl Entomol Zool 40:47CrossRefGoogle Scholar
  79. Kovalev AE, Varenberg M, Gorb SN (2012) Wet versus dry adhesion of biomimetic mushroom-shaped microstructures. Soft Matter 8:7560CrossRefGoogle Scholar
  80. Kwak MK, Pang C, Jeong HE, Kim HN, Yoon H, Jung HS, Suh KY (2011) Towards the next level of bioinspired dry adhesives: new designs and applications. Adv Funct Mater 21:3606CrossRefGoogle Scholar
  81. Langer MG, Ruppersberg JP, Gorb SN (2004) Adhesion forces measured at the level of a terminal plate of the fly’s seta. Proc R Soc Lond B 271:2209CrossRefGoogle Scholar
  82. Murphy MP, Aksak B, Sitti M (2007) Adhesion and anisotropic friction enhancements of angled heterogeneous micro-fiber arrays with spherical and spatula tips. J Adhes Sci Tech 21:1281CrossRefGoogle Scholar
  83. Niederegger S, Gorb SN (2003) Tarsal movements in flies during leg attachment and detachment on a smooth substrate. J Insect Physiol 49:611CrossRefGoogle Scholar
  84. Niederegger S, Gorb SN (2006) Friction and adhesion in the tarsal and metatarsal scopulae of spiders. J Comp Physiol A 192:1223CrossRefGoogle Scholar
  85. Niederegger S, Gorb SN, Vötsch W (2001) Fly walking: a compromise between attachment and motion? In: Wisser A, Nachtigall W (eds) Technische Biologie und Bionik. 5. Bionik – Kongress, Dessau 2000. Gustav Fisher Verlag, Stuttgart/Jena/Lübeck/Ulm, pp 327–330Google Scholar
  86. Niewiarowski PH, Lopez S, Ge L, Hagan E, Dhinojwala A (2008) Sticky gecko feet: the role of temperature and humidity. PLoS One 3:e2192CrossRefGoogle Scholar
  87. Northen MT, Turner KL (2005) A batch fabricated biomimetic dry adhesive. Nanotechnology 16:1159CrossRefGoogle Scholar
  88. Peattie AM, Full RJ (2007) Phylogenetic analysis of the scaling of wet and dry biological fibrillar adhesives. Proc Natl Acad Sci U S A 104:18595CrossRefGoogle Scholar
  89. Peisker H, Gorb SN (2012) Evaporation dynamics of tarsal liquid footprints in flies (Calliphora vicina) and beetles (Coccinella septempunctata). J Exp Biol 215:1266CrossRefGoogle Scholar
  90. Peisker H, Michels J, Gorb SN (2013) Evidence for a material gradient in the adhesive tarsal setae of the ladybird beetle Coccinella septempunctata. Nat Commun 4:1661CrossRefGoogle Scholar
  91. Peisker H, Heepe L, Kovalev AE, Gorb SN (2014) Comparative study of the fluid viscosity in tarsal hairy attachment systems of flies and beetles. J R Soc Interface 11:20140752CrossRefGoogle Scholar
  92. Pelletier Y, Smilowitz Z (1987) Specialized tarsal hairs on adult male Colorado potato beetles, Leptinotarsa decemlineata (Say), hamper its locomotion on smooth surfaces. Can Entomol 119:1139CrossRefGoogle Scholar
  93. Peressadko A, Gorb SN (2004a) When less is more: experimental evidence for tenacity enhancement by division of contact area. J Adhes 80:247CrossRefGoogle Scholar
  94. Peressadko A, Gorb SN (2004b) Surface profile and friction force generated by insects. In: Fortschritt-Berichte VDI, Boblan I, Bannasch R (eds) Surface profile and friction force generated by insects, vol 249[15]. VDI Verlag, Düsseldorf, pp 257–263Google Scholar
  95. Persson BNJ (2003) On the mechanism of adhesion in biological systems. J Chem Phys 118:7614CrossRefGoogle Scholar
  96. Persson BNJ (2014) On the fractal dimension of rough surfaces. Tribol Lett 54:99CrossRefGoogle Scholar
  97. Persson BNJ, Gorb SN (2003) The effect of surface roughness on the adhesion of elastic plates with application to biological systems. J Chem Phys 119:11437CrossRefGoogle Scholar
  98. Popov VL (2010) Contact mechanics and friction: physical principles and applications. Springer-Verlag, BerlinzbMATHCrossRefGoogle Scholar
  99. Prowse MS, Wilkinson M, Puthoff JB, Mayer G, Autumn K (2011) Effects of humidity on the mechanical properties of gecko setae. Acta Biomater 7:733CrossRefGoogle Scholar
  100. Pugno NM (2011) The theory of multiple peeling. Int J Fract 171:185CrossRefGoogle Scholar
  101. Pugno NM, Gorb SN (2009) Functional mechanism of biological adhesive systems described by multiple peeling approach. In: Proceedings of the 12th international conference on fracture, July 1217, OttawaGoogle Scholar
  102. Puthoff JB, Prowse MS, Wilkinson M, Autumn K (2010) Changes in materials properties explain the effects of humidity on gecko adhesion. J Exp Biol 213:3699CrossRefGoogle Scholar
  103. Richards AG, Richards PA (1979) The cuticular protuberances of insects. Int J Insect Morphol Embryol 8:143CrossRefGoogle Scholar
  104. Rizzo NW, Gardner KH, Walls D, Keiper-Hrynko JNM, Ganzke TS, Hallahan DL (2006) Characterization of the structure and composition of gecko adhesive setae. J R Soc Interface 3:441CrossRefGoogle Scholar
  105. Röll B (1995) Epidermal fine structure of the toe tips of Sphaerodactylus cinereus (Reptilia, Gekkonidae). J Zool 235:289CrossRefGoogle Scholar
  106. Ruibal R, Ernst V (1965) The structure of the digital setae of lizards. J Morphol 117:271CrossRefGoogle Scholar
  107. Russell AP (1975) A contribution to the functional analysis of the foot of the Tokay, Gekko gecko (Reptilia: Gekkonidae). J Zool (Lond) 176:437CrossRefGoogle Scholar
  108. Sameoto D, Menon C (2010) Recent advances in the fabrication and adhesion testing of biomimetic dry adhesives. Smart Mater Struct 19:103001CrossRefGoogle Scholar
  109. Schargott M (2009) A mechanical model of biomimetic adhesive pads with tilted and hierarchical structures. Bioinspir Biomim 4(026002):9Google Scholar
  110. Scherge M, Gorb SN (2001) Biological micro- and nanotribology: nature’s solutions. Springer, BerlinCrossRefGoogle Scholar
  111. Schleich HH, Kastle W (1986) Ultrastrukturen an Gecko-Zehen (reptilia: sauria: gekkonidae). Amphibia-Reptilia 7:141CrossRefGoogle Scholar
  112. Sitti M, Fearing RS (2003) Synthetic gecko foot-hair micro/nano-structures as dry adhesives. J Adhes Sci Technol 17:1055CrossRefGoogle Scholar
  113. Smith JM, Barnes WJP, Downie JR, Ruxton GD (2006) Structural correlates of increased adhesive efficiency with adult size in the toe pads of hylid tree frogs. J Comp Physiol A 192:1193CrossRefGoogle Scholar
  114. Spolenak R, Gorb SN, Gao H, Arzt E (2005) Effects of contact shape on the scaling of biological attachments. Proc R Soc Lond A 461:305CrossRefGoogle Scholar
  115. Stork NE (1980a) Experimental analysis of adhesion of Chrysolina polita (Chrysomelidae: Coleoptera) on a variety of surfaces. J Exp Biol 88:91Google Scholar
  116. Stork NE (1980b) A scanning electron microscope study of tarsal adhesive setae in the Coleoptera. Zool J Linnean Soc 68:173CrossRefGoogle Scholar
  117. Stork NE (1983) A comparison of the adhesive setae on the feet of lizards and arthropods. J Nat Hist 17:829CrossRefGoogle Scholar
  118. Tang T, Hui CY (2005) Can a fibrillar interface be stronger and tougher than a non-fibrillar one? J R Soc Interface 2:505CrossRefGoogle Scholar
  119. Varenberg M, Gorb SN (2008a) A beetle-inspired solution for underwater adhesion. J R Soc Interface 5:383CrossRefGoogle Scholar
  120. Varenberg M, Gorb SN (2008b) Close-up of mushroom-shaped fibrillar adhesive microstructure: contact element behaviour. J R Soc Interface 5:785CrossRefGoogle Scholar
  121. Varenberg M, Gorb SN (2008c) Shearing of fibrillar adhesive microstructure: friction and shear-related changes in pull-off force. J R Soc Interface 4:721CrossRefGoogle Scholar
  122. Varenberg M, Pugno NM, Gorb SN (2010) Spatulate structures in biological fibrillar adhesion. Soft Matter 6:3269CrossRefGoogle Scholar
  123. Varenberg M, Murarash B, Kligermann Y, Gorb SN (2011) Geometry-controlled adhesion: revisiting the contact splitting hypothesis. Appl Phys A Mater Sci Process 103:933CrossRefGoogle Scholar
  124. Voigt D, Schuppert JM, Dattinger S, Gorb SN (2008) Sexual dimorphism in the attachment ability of the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) to rough substrates. J Insect Physiol 54:765CrossRefGoogle Scholar
  125. Vötsch W, Nicholson G, Müller R, Stierhof Y-D, Gorb SN, Schwarz U (2002) Chemical composition of the attachment pad secretion of the locust Locusta migratoria. Insect Biochem Mol Biol 32:1605CrossRefGoogle Scholar
  126. Walker G, Yulf AB, Ratcliffe J (1985) The adhesive organ of the blowfly, Calliphora vomitoria: a functional approach (Diptera: Calliphoridae). J Zool (Lond) 205:297CrossRefGoogle Scholar
  127. Wigglesworth VB (1987) How does a fly cling to the under surface of a glass sheet? J Exp Biol 129:373Google Scholar
  128. Wolff JO, Gorb SN (2011) The influence of humidity on the attachment ability of the spider Philodromus dispar (Araneae, Philodromidae). Proc R Soc London, Ser B 279:139CrossRefGoogle Scholar
  129. Wolff JO, Gorb SN (2012) Surface roughness effects on attachment ability of the spider Philodromus dispar (Araneae, Philodromidae). J Exp Biol 215:179CrossRefGoogle Scholar
  130. Wolff JO, Gorb SN (2016) Attachment structures and adhesive secretions in arachnids. Springer, BerlinCrossRefGoogle Scholar
  131. Yurdumakan B, Raravikar NR, Ajayan PM, Dhinojwala A (2005) Synthetic gecko foot-hairs from multiwalled carbon nanotubes. Chem Commun 16041421:3799CrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Functional Morphology and BiomechanicsZoological Institute at the University of KielKielGermany

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