Biological Fibrillar Adhesives: Functional Principles and Biomimetic Applications
- 331 Downloads
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.
KeywordsAttachment Biomimetics Bioinspired surfaces Microstructure Fibrillar adhesives Dry adhesives Dynamic adhesion Reversible adhesion Bioadhesion Microfabrication Gecko Insect Spider
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.
2 Dynamic Adhesion for Locomotion
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).
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
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
6 Contact Shape
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).
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
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
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.
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
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
Anisotropic attachment: Attachment force variable depending on the setal-spatula orientation with respect to the substrate, normal load, and parallel drag.
High adhesion coefficient: Ratio of preload to pull-off force, which represents the strength of adhesion as a function of the compressive load.
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.
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.
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.
Anti-self-adhesion: Hierarchical fibrillar structure avoids the self-adhesion of individual structural elements.
- 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.
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.
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.
Real biological attachment systems usually rely on the combination of different functional principles based on elaborate micro- and nanostructures.
Attachment systems in biology can be subdivided according to their structure and basic physical forces responsible for enhancement of contact forces.
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.
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.).
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).
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.
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.
Hierarchical organization of surface features in attachment pads may enhance adaptability to real surfaces, which often have fractal roughness.
Asymmetrical shape of single contact element (tilted position relative to the support) in combination with proper movements may provide a way to switchable adhesives.
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.
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.
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.
- 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
- 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
- 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
- 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
- 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
- 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
- Edwards JS, Tarkanian M (1970) The adhesive pads of Heteroptera: a re-examination. Proc Roy Ent Soc Lond A 45:1Google Scholar
- Gorb SN (2001) Attachment devices of insect cuticle. Springer, New YorkGoogle Scholar
- 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
- 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
- Gottlieb Binder GmbH & Co KG (2017) http://www.binder.de/en/products/geckonanoplast/
- 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
- Israelachvili JN (1992) Intermolecular and surface forces: With Applications to Colloidal and Biological Systems, 2nd edn. Academic, LondonGoogle Scholar
- 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
- 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
- Kim S, Sitti M (2006) Biologically inspired polymer microfibers with spatulate tips as repeatable fibrillar adhesives. Appl Phys Lett 89:26911Google Scholar
- 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
- 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
- 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. VDI Verlag, Düsseldorf, pp 257–263Google Scholar
- 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
- Schargott M (2009) A mechanical model of biomimetic adhesive pads with tilted and hierarchical structures. Bioinspir Biomim 4(026002):9Google Scholar
- Stork NE (1980a) Experimental analysis of adhesion of Chrysolina polita (Chrysomelidae: Coleoptera) on a variety of surfaces. J Exp Biol 88:91Google Scholar
- Wigglesworth VB (1987) How does a fly cling to the under surface of a glass sheet? J Exp Biol 129:373Google Scholar