Fold Hybrid Structure-Based Fluidic Networks Inspired by the

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Crack/Fold Hybrid Structure based Fluidic Networks Inspired by the Epidermis of Desert Lizards Junghwa Cha, Hyunjae Shin, and Pilnam Kim ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.6b10862 • Publication Date (Web): 05 Oct 2016 Downloaded from http://pubs.acs.org on October 13, 2016

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ACS Applied Materials & Interfaces

Crack/Fold Hybrid Structure based Fluidic Networks Inspired by the Epidermis of Desert Lizards Junghwa Cha, Hyunjae Shin and Pilnam Kim* Department of Bio and Brain Engineering, KAIST, Daejeon, 34141, Korea KEYWORDS Cracks, Fold, Scales, semi-tubular structure, Bio-inspired system, Shape-tunable fluidic networks

ABSTRACT

A bioinspired fluidic system with cracks and folds was introduced to emulate the structures and functions of desert lizards’ integuments, which show marked ability of water management. Since there was a structural analogy between scales and interscalar channels of lizard’s skin and cracks and folds of a bilayer elastic material, we can mimic lizard’s skin by controlling the stress distribution on patterned elastomers. Our system showed not only capillary-driven water retention within confined fluidic network, but also stretching-driven biaxial water transport. Observed features of our system may enhance understanding of water management in relation to morphogenetic aspects of lizards.

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Natural creatures living in arid environments have developed a diverse range of water management strategies, evolving various integument structures including wrinkles, grooves and cracks that act as water transport channels.1 Using such strategies, some desert creatures can transport water spontaneously, and do not require external sources of water uptake. Beetles in the Namib Desert, for instance, utilize hydrophilic–hydrophobic microbumps on their backs to collect water droplets from the morning fog.2-3 The wharf roach is reported to transport water through capillaries with a wettability-modified surface on its legs.4 Desert lizards, including the Australian thorny devil and Texas horned lizards, transport water to their mouths using interconnected capillary systems formed in their folded epidermis, which exhibits superhydrophilicity.5-6 Despite the existence of these naturally occurring, well-defined wettingcontrolled strategies for water transport,7-10 to the best of our knowledge, little is known about the morphogenetic aspects of water management systems, and consequently little is revealed about the functioning of these systems. Here, we first discuss the formation of a bioinspired crack/fold hybrid structure based fluidic system, which mimics the integuments of desert lizards. We then investigate the morphological contribution of the system for fluidic control. The scaled epidermis of desert lizards consists of three layers: β-keratin, mesos, and α-keratin layers (Figure 1A). Structurally, outer β-keratin layer is composed of rigid proteins, whereas inner α-keratin layer is composed of more flexible proteins.11 The layered epidermis of lizards develops folded structures with scales.6, 11 These interscalar channels and scales are interconnected via a semi-tubular capillary system, enabling capillary-driven control over the flow of water.6 Inspired by these integuments of the layered epidermis of lizards, we fabricated bioinspired crack/fold hybrid structure based fluidic systems using layered elastic polydimethylsiloxane (PDMS) membranes. This mimics two main


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components of the lizard’s semi-tubular capillary system; i.e., the scales are mimicked by open channels and the interscalar channels by semi-closed channels (Figure 1B). When a bilayer system composed of a relatively stiff, thin film bonded to compliant substrates is compressed, the morphology of the film changes into well-defined sinusoidal wrinkles or sharp folds, and even cracks are formed orthogonal to the direction of the applied strain.12-15 The geometry of the folds (or wrinkles), as well as that of the cracks, can be controlled by varying the mechanical, geometrical and loading parameters.16-20 Notch-mediated crack formation, for instance, is one of methods to control mechanical fractures by focusing stress, hence guiding crack formation.16-17,

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Micronotches on an elastomeric bilayer can act to control crack

formation; i.e., the deformation energy can be localized (or focused) at pre-defined positions during compression, thereby controlling the formation of cracks. Similarly, folds can evolve in a spatially controlled manner by applying a pre-patterned groove structure. Using such a prepatterned structure, we fabricated notch-mediated cracks and groove-mediated controlled folds to form open and semi-closed channels, respectively. Figure 2A shows an illustration of the process used to fabricate the bioinspired water management system, which mimics the lizard’s scaled semi-tubular fluidic networks. Using photolithography, we defined 5-µm-depth microgrooves, where the grooves were 3-µm-width and the ridges were 10-µm-width. In addition, we arrayed v-shaped micronotches at every 100µm interval on ridges of the microgrooves, of which trapezoidal sides were in 3-µm and 2-µm

and height was 4-µm, resulting in the local area with 2-µm-width and 2-µm-height (Figure S1A). We then applied uniaxial strains on patterned elastomer in the range 45–75% in the x-direction (see the black arrow in Figure S1A), and subsequently oxidized the elastomer using ultraviolet/ozone (UVO) for 30 min (Figure 2A-2). Following UVO exposure, the surface of the


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PDMS elastomer developed a silica-like stiff film. Due to the layered thin-film structure of the elastomer, when the strain was released (see the gray arrow in Figure 2A-2), the film began to form a uniform distribution of folds perpendicular to the direction of the applied strain, with cracks that formed perpendicular to the folds (Figure 2A-3). We were able to obtain a bioinspired crack/fold hybrid structure based fluidic system consisting of both cracks (open channels) and folds (semi-closed channels) to mimic the structure of lizard skin (Figure 2A-4). We calculated the stress distribution on the pre-patterned PDMS membrane surfaces using the finite element method (FEM) (Figs. 2B, 2C and S1B). Using the same geometric parameters that were used in the experiments, we modeled a patterned two-dimensional PDMS surface (with a Young’s Modulus of 2 MPa). As expected, following the application of 45–75% uniaxial strain, the tensile stress became localized at the micronotches (see the red features in Figure 2B and S1B), and the compressive stress concentrated between the grooves (see the blue features in Figure 2B and S1B). With a pre-applied strain of 0.75, both the tensile and compressive stresses intensified. Compared with the average stress at the 10-µm-wide ridges (0.158 MPa, reference stress at the ridge, σref), on average the tensile stress was 0.374 MPa at the edge of micronotches. The stress concentration factor Kt, defined as the ratio of the maximum tensile stress to the reference stress (i.e., σmax/σref), was 2.37; i.e., the stress intensified at notches by a factor of 2.37, and a compressive stress of 0.504 MPa was localized at the 3-µm-wide grooves. Scanning electron microscope (SEM) images showed that cracks developed in the x-direction and folds developed in the y-direction (Figure 2D-a). Cross-sectional images of the outer crack structures and the inner folded channels revealed that the v-shaped microstructure of the cracks was obtained by tearing the micronotches following stress concentration (Figure 2D-b) and a sharp structure of the nanoscale folds was observed between the grooves (Figure 2D-c). In this


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manner, the formation of both cracks and folds could be controlled based on the initial pre-strain (Figure S1C). As the extent of this pre-strain increased, the crack density increased at the notches, and the periodicity of the folds decreased. The features of the cracks and folds were carefully inspected as the pitch of the patterned notches was varied. The micronotches were arrayed according to a longitudinal interval that varied in the range 10–100 µm, and the microgroove geometry was fixed with 10-µm-wide ridges and 3-µm-wide grooves (Figure 2E and S2A). For all pre-strains (i.e., 45–75%), the crack density increased in proportion to the notch interval (Figure 2E). Moreover, greater pre-strain resulted in a larger crack density. With a pre-strain of 75%, cracks formed with a longitudinal interval of 50 µm (Figure 2E and S2A). The size of the cracks was proportional to the pre-strain (Figure S2B). The resulting cracks were larger than the initial geometry of the micronotches (5– 13 µm, compared with the 2-µm-wide and 2-µm-high micronotches). We investigated the simultaneous formation of folded channels on a patterned elastomer with 50 µm notch intervals. With these folded channels, semi-closed channels were clearly formed at the nanoscale for all pre-strains, with periodic folds (Figure 2F). The periodicity of the folds decreased as the pre-strain increased. Interestingly, for pre-strains in the range 0–75%, only wrinkles formed on the unpatterned (flat) elastomer, with no folds (Figure S3A). Using an analytical model, we found that the presence of patterned microgrooves on the surface resulted in regular regions of strain concentration, whereas the strain distribution was constant on the planar (unpatterned) surface (Figure S3B). Thus, the folds occurred at the pre-patterned locations. Based on these results, it appears that open cracks and semi-closed folds can be precisely controlled via predefined micronotches and microgroove structures.


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We then evaluated the role of the cracks and folds in water management, as open and semiclosed channels. We used pre-patterned PDMS surfaces with 50 µm micronotch intervals, and fabricated crack/fold hybrid structure based fluidic systems. To investigate the water-retention properties of the system, 5-µL water droplets with fluorescent dye (0.05% rhodamine B) were introduced on the surface of the samples (Figure 3A). Due to the UVO-treatment during fabrication, the fluorescent dye droplets were immediately spread and retained on the cracks (i.e., open channels) (Figure 3A-a). The fluid was then absorbed into the inner folded channels (Figure 3A-b) via capillary action. We quantified the average flow rate of water absorption (Figure S4). The inner folded channel was sufficiently filled within 3 min, consistent with the results obtained using Washburn’s equation; 2 + ∙ cos () ∙ ( + 4 ) = ~145 nm/s 8 where l is length of the capillaries (50 µm), t is time, r is the radius of the capillaries (20 nm), P0 is the external pressure (0 Pa), γ is the surface tension (72.5 mN/m), φ is the contact angle (60°), η is the viscosity of the water (1 mPas) and ε is the coefficient of slip (0.1). Figure 3B shows representative experimental images of water retention in the fluidic system. Following incubation for 5 min, with the 45% and 60% pre-strained surfaces, red fluorescent signals from the semi-closed channels were detected only in the presence of open crack channels, due to sequential water transport from open to semi-closed channels. For 75% pre-strain, red signals were detected over all of the semi-closed folded channels. In this process, water is transported spontaneously from the microscale open channels to the nanoscale semi-closed channels via capillary forces.


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To quantify the water retention, we incubated 5-µL water droplets for 5 min, and then removed the residual water from the surfaces. By measuring the change in mass (Figure 3C), we found that the water retention ability with a pre-strain of 75% was 7 mg, which was significantly greater than that for pre-strains of 45% and 60% (1–2 mg). These results indicate that the semiclosed channels acted as voids for water adsorption, similar to the interscalar voids beneath the scales of lizards, and filled with water via capillary action. Thus, the inner folded channels have potential applications for water retention systems that mimic the water-retaining ability of the epidermal folds of lizards. In addition to the water retention properties, there have been reports of water transport by lizards during drinking. It appears that lizards transport water to their mouths via capillary action, against gravity, and with controlled direction of flow.11 In addition to the capillary-induced transport, it has been theorized that this directional, pan-cutaneous flow of water within the lizard is accomplished via channels, rather than scales.6 This may be because the flow in the channels results from a pressure difference between the skin and the mouth.6,

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The mechanisms of

directional water transport have been explained using biomimetic systems such as microstructured surfaces21-23 and porous fabrics.24-26 These reports focused on the wettability or on surface-tension-mediated water transport; however, it appears that these biological systems regulate fluid flow using deformable channels or tubes.27-28 In such systems, interactions between the fluid flow and elastic deformation of the channels can lead to a variety of significant transport phenomena.29-30 The feasibility of shape-tunable fluidic networks for directing and controlling water transport has not previously been demonstrated. We thus investigated the mechanism of water transport in our crack/fold hybrid structure based networks by controlling the geometry.


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Because of the elasticity of the system, we can modulate the configuration of the cracks and folded channels by applying mechanical strain (Figure 4A). This strain-based shape tunability of the channel networks was observed using a phase-contrast microscope (Figure 4B). The folds were initially semi-closed, and the cracks were open. Following the application of tensile strain, the folds opened, and the cracks closed. During this process, we observed that the directionality of fluid flow depended on the strain; i.e., initially, water was retained within the semi-closed channels, but after applying strain, the water flowed into the open channels. These results demonstrate that water flow within the system can be modulated by controlling the shapes of the cracks and folds in the interconnected network by applying mechanical strain. To further investigate modulation of the fluid flow within the system, we visualized the movement of microbeads during the application of tensile strain. Initially, the microbeads were randomly distributed across the surface (Figure 4C-b and 4D-b), but when the system was stretched, the microbeads moved along the folds and were captured in the closing cracks (Figure 4C-c and 4D-c). Moreover, this was reversible; because of the elasticity of the system, we could repeatedly modulate the shape of both types of channel by straining and releasing the elastomeric system. When microbeads were captured by the closing cracks in the tensile-strained condition, they remained in the cracks following release of the strain (Figure 4D-b’), whereas the fluid flow was reversible. These results show that fluid flow within the system could be modulated by the tunable configuration of the elastic, and by the network of cracks and folds, which suggests that shape-deformation-mediated water transport is feasible. In summary, we generated crack/fold hybrid structure based fluidic networks via controlled formation of cracks and folds, induced by applying mechanical strain. By patterning the surfaces with micronotches and grooved structures, we could fabricate microscopic architectures that


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mimicked the open and semi-closed channels of desert lizards. Using this networked system, we confirmed the feasibility of surface-tension-driven water retention and transport within the confined fluid network. Due to the interconnected cracks and folds, water could be spontaneously transported into the inner folded channels from the surface cracks via capillary action. In addition, because of the shape tunability of both the cracks and folds, the fluidic network (and hence the flow of water) could be modulated by applying mechanical strain. Such control over fluid transport can be used as a mechanism for water transport systems. Our bioinspired system may therefore contribute not only to our understanding of the water transport that occurs when lizards drink, but may also provide opportunities for directing fluid within confined microfluidics systems.


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ASSOCIATED CONTENT Supporting Information. The supporting Information is available free of charge via the Internet at http://pubs.acs.org. Detailed information for materials and fabricating procedures and corresponding analysis methods. AUTHOR INFORMATION Corresponding Author *Pilnam Kim. E-mail: [email protected] Notes The authors declare no competing financial interest. ACKNOWLEDGMENT This research was supported from the National Research Foundation of Korea (NRF) (grant number : NRF-2015H1A2A1030560, NRF-2014M3C1B2048201 and NRF 35B-2011–1D00013).


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Table of Contents

Water managing fluidic networks inspired by the epidermis of desert lizards are developed using layered elastomer. By controlling the formation of cracks and folds as analogy of scales and interscalar channels in lizards, the scaled semi-tubular fluidic networks were fabricated under the compressive strains. The flow in fluidic networks was retained and mechanically tuned, which resembles lizard’s water retention ability.


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Figure 1. (A) Integuments of desert lizards. The scaled epidermis consists of three layers: β-keratin, mesos, and α-keratin. (B) Comparison between the layered epidermis of desert lizards for drinking water, and the layered elastomeric water management system. Both feature networks of open and semi-closed channels. 188x153mm (150 x 150 DPI)


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Figure 2. (A) An illustration of the fabrication process for the bioinspired crack/fold hybrid structure based fluidic system. Pre-patterned PDMS (1) is stretched and then UV/ozone-exposed (2). When releasing (3), the surface of PDMS results in the folded structures, simultaneously initiating the cracks (4). (B) Stress distribution on the pre-patterned surfaces. Top-views of the pre-patterned elastomer (left) and the fabricated elastomer (right), as well as stress concentration (middle). (Scale bar: 250 µm) (C) Localized stresses at the surfaces. The maximum stress was calculated at the micronotches, and compared with the reference stress at a cross-section containing only microgroove patterns. (D) Simultaneous formation of cracks and folds shown in a perspective view (a). Cross-sectional views of the V-shaped cracks (b) and semi-tubular folds (c). (E) Crack formation with various notch intervals. (F) The periodic structures of the folds following pre-straining (black: 45% pre-strain; blue: 60% pre-strain; and red: 75% pre-strain). 190x235mm (150 x 150 DPI)



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Figure 3. Water retention in the bioinspired crack/fold hybrid structure based fluidic system. (A) A schematic diagram showing the water retention process. Water is first retained within the open cracks (a), and then absorbed into the semi-closed folded channels (b). (B) Representative images of water containing rhodamine B dye retained within the system. Scale bar: 100 µm. (C) Quantification of the water retention ability of the system. The asterisk indicates statistical significance (*p

Fold Hybrid Structure-Based Fluidic Networks Inspired by the

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