It is noteworthy that the characteristic geometry and structure of the internal tissue in the remora suction disc have been rarely reported. Among other adhesive tissues, the octopus sucker tissue is more like active muscles arranged in a complex 3D array (radial, meridional, and circular), providing skeletal-like support for adhesion.The toe pad of tree frog presents a different morphology of sparsely distributed collagen and elastic fibers in the dermis, but the orientation of fibers has not yet been characterized.It is proposed that the remora's unique tissue morphology of vertical fibers relative to the contact surface is important to the adhesion function, and we explore its structure-property-function relationship further through biomimetics and by engineering a synthetic prototype as follows.

Morphological studies of the toe pads of the rock frog, Staurois parvus (family: Ranidae) and their relevance to the development of new biomimetically inspired reversible adhesives.

According to the histology and scanning electron microscopy (SEM) images, the remora lip tissue can be modeled as three layers, corresponding to varied material morphology and mechanical role. The cross-sectional schematic view is illustrated in Figure 1 B: (1) the outermost skin layer, (2) the under-skin layer, and (3) the central tissue section. The skin layer to directly contact the host appears rough on the surface and ∼30 μm thin ( Figure S1 ). The under-skin layer is ∼250–500 μm thin, with layered horizontally compact collagen bundles (∼40–60 μm in diameter) (black arrows in Figures 1 F–1H). In contrast, the central tissue section shows a distinctive cross-sectional morphology with vertically arranged and crimped/relaxed collagen fibers (5–15 μm in diameter and 300–550 μm in length, indicated by red arrows in Figures 1 F–1K). This central tissue constitutes up to ∼60% of the thickness of the whole lip tissue. These central collagen fibers extend from both sides of the horizontal under-skin layer without a clear borderline, perpendicular to the inner and outer skin layer.

The surrounding, soft suction disc of remora is oval-shaped and the cross-section of the disc is wedge-shaped ( Figure 1 A). The histology images show clear characteristics of connective tissue ( Figures 1 C–1H), consisting of cells and an extracellular matrix (ECM) consisting of unique fibrous structure ( Figure S1 ), whose main component is abundant, dense, coarse, and well-aligned collagen fibers, distributed in different layers. The Verhoeff Van Gieson (EVG) staining results also reveal that the ECM contains a little elastin ( Figure S1A ). The lip tissue is highly hydrated and the water content is estimated at around 84.4% ± 2.7% by weighing the wet/dry mass.

The nylon fiber flocked silicone was then embedded into a 3D-printed mold, which was filled with uncured silicone elastomer. The curing reactions that release heat and reduce the volume of the composite also enhance the fiber-matrix interfacial contact. A biomimetic disc prototype was eventually successfully fabricated, whose geometrical features were similar to that of the natural counterpart ( Figure S4 Tables S1 and S2 ). The SEM images of the cross-sectional view show vertically standing fibers ( Figures 2 C and 2D) and the seamless contact between nylon fibers and silicone matrix in the biomimetic remora disc lip (inset image of Figure 2 C).

A number of strategies to mimic biological structures with controlled fiber alignment have been developed, including electrospinning,woven fabric,and 3D-printing techniques assisted by shear forces,electric fields,and magnetic fields.However, we focus on mimicking the unique structure of remora disc lip with relatively large size (length ≥300 μm) and vertically oriented fibers inside a planar substrate. In this work, we applied electrostatic flockingto insert massive, short artificial fibers vertically onto a soft substrate to create a biomimetic tissue composite. The principle is electrostatic attraction and utilizing a controllable electric field to align conductive fibers vertically onto a receiving substrate ( Figure 2 A). Here we used nylon 66 fibers (elastic modulus E ∼ 2 GPa, Figure S2 ), which are commonly used and widely available as reinforcement for soft matrices in composites.Vertical nylon fibers were placed onto a 500-μm-thick silicone layer (Ecoflex 0020, E ∼ 55 kPa), and the morphology of the resultant nylon fibers flocked silicone is shown in Figure 2 B, indicating that the vertically aligned fibers are well fixed into the silicone substrate. In our experiment, the flocking density can reach ∼120 fibers/mm(about 8% estimated from cross-sectional area analysis) in seconds under 500 kV/m electric field. The electrostatic flocking equipment and the process of the electrostatic flocking can be seen in Figure S3 and Video S1 , respectively.

(C and D) Transverse section (C) and longitudinal section (D) of the nylon fiber/silicone composite. Circle and arrow indicate the fiber orientation. Scale bars, 100 μm. The inset in (C) highlights the well-adhered fiber-matrix interface (scale bar, 20 μm).

(B) Microscopic morphology of nylon fiber flocked silicone (side view). The vertical and horizontal arrows indicate the fiber orientation relative to the silicone substrate. Scale bar, 500 μm.

Fabrication and Morphology of Biomimetic Composite from Nylon Fiber and Silicone for the Suction Disc

Figure 2 Fabrication and Morphology of Biomimetic Composite from Nylon Fiber and Silicone for the Suction Disc

Effects of nanoclay and short nylon fiber on morphology and mechanical properties of nanocomposites based on NR/SBR.

The tensile creep behaviors of natural lip tissue, pure rubber matrix, and composite were examined for a 30-min creep under 10 kPa tensile stress and 30 min of recovery ( Figure 3 F). After applying the tensile stress, the rubber matrix, natural tissue, and the composite displayed a sharp elastic strain εand a slow viscous εas a function of time. After unloading, the elastic strain instantly recovered and the viscous strain slowly decreased. The fast equilibrium of creep strain helps to resist the deformation under the drag of the host, which was specifically reflected in less overall strain, less viscous strain, and less unrecovered strain. We applied the Burgers model to analyze the tensile creep behavior ( STAR Methods ). The experimental creep data in Figure 3 F were fitted with the Burgers model with R> 0.96, and the four parameters are summarized in Table S3 . The fitting results indicate that the composite had elastic modulus E= 891 kPa, which is ∼10-fold that of pure silicone rubber. This is consistent with the quasi-static tensile test results. The retardation time τ for the viscoelastic element followed the order τ(composite) < τ(natural tissue) < τ(rubber). In general, the greater elastic moduli, shorter retardation time, and lower viscosity of the biomimetic lip composite could lead to a more solid-like creep behavior, which could benefit the hitchhiking of remora, e.g., by helping to maintain the internal negative pressure and, thus, the adhesive force.

In addition, the mechanical properties of natural remora disc lip tissue are frequency dependent, as shown in Figure S8A . As the compression frequency increases, both storage modulus E′ and loss modulus E″ increase. E′ increases from 20 to 90 kPa and E″ increases from 10 to 25 kPa for two decades of frequency increase. Furthermore, the loading-unloading curve ( Figure S8B ) shows an apparent hysteresis loop, indicating that the natural lip tissue can dissipate up to ∼70% energy at a compressive stress of 5 kPa.

The cyclical vertical compressive creep behavior is shown in Figure 3 E. Throughout the repetitive (100 times) compressive loadings-unloadings (10 kPa), the creep strain of each cycle is consistent and stable. This means the natural tissue can sustain periodic loadings at stress levels of 10 kPa and behave reliably to ensure numerous episodes of adhesion during remora's lifetime.

Natural tissues and biomimetic synthetics made from polymers commonly feature viscoelasticity and time-dependent mechanical behavior. Thus, we also performed loading/unloading cyclical tests, creep tests, and dynamic tests of varying frequencies to reveal the materials' structure and property change as a function of time/frequency. Figure 3 D displays the creep curves of the natural lip tissue under 1, 5, 10, and 20 kPa compressive stress in the vertical direction. Lip tissues were subject to a 60-min loading followed by a 10-min recovery. After applying the stress, the lip tissue immediately recovers with a sharp elastic strain, and the viscous strain gradually develops in ∼10 min until reaching a plateau strain. As the creep stress increases, the characteristic time to reach the plateau strain increases. The slope for the strain/stress trendline also decreases ( Figure S7 ), indicating a stiffening effect under increased compressive stress.

For the biomimetic tissue composite, the quasi-static mechanical properties of the vertical nylon-fiber-reinforced silicone were also characterized in three directions under tensile/compression ( Figure 3 B). The tensile modulus ( Table 1 and Figure 3 C) of the synthetic composite are 62 ± 7 kPa, 78 ± 15 kPa, and 1,013 ± 435 kPa in circumferential, radial, and vertical directions, respectively. The vertical tension modulus of the synthetic composite is 10- to 20-fold higher than the circumferential and radial modulus, as well as the vertical compression modulus (74 ± 8 kPa). Mechanical anisotropy is clearly realized in the synthetic counterpart. Compared with isotropic pure matrix (Ecoflex silicone, E ∼ 55 kPa), the biomimetic composite with aligned nylon fibers mimics the vertical fibrous morphology of the natural remora disc lip tissue and emulates the anisotropic mechanical characteristics. The finite element modeling (FEM) results also show the contribution of fibers to increasing vertical tensile modulus and limiting tensile deformation, as the value of σ(equivalent stress) on fibers was higher than that of silicone matrix ( Figure S6 ).

Clearly, the mechanical characteristics of remora lip tissue are a result of the distinctive fibrous architecture and structural anisotropy. The vertically standing collagen fibers in the central section lead to high vertical tensile modulus and low compressive modulus due to buckling and crimping, and the woven collagen fibers in the under-skin layer can resist tensile deformation and lead to a comparable tensile modulus on the circumferential and radial direction. In addition, the strain-hardening behavior in circumferential and radial directions may be explained by the crimped skin layers. Figure S1A provides a measurement of the wavy and straightened lengths of the superficial under-skin layer, corresponding well to the start of strain hardening (from ∼15% to 35%). When fibers are straightened, the tension changes from stretching out the fiber waves to directly stretching the fibers, indicating significant stiffening. The cyclical creep curve of lip tissue in circumferential tension under 200 kPa also proved the strain-hardening effect ( Figure S5 ).

We firstly evaluated the quasi-static mechanical properties of both natural and biomimetic lip materials. Tension tests perpendicular to/along the fiber axis and compression tests along the fiber axis were conducted. The representative tensile stress-strain curves of natural remora disc lip tissue in three directions and the compressive stress-strain curve in the fiber axis (V direction) are plotted in Figure 3 A. The mechanical properties (modulus, breaking strain, and breaking stress) are summarized in Table 1 . The tensile stress-strain responses display non-linear and inelastic behaviors, and tensile responses along the circumferential and radial directions are very similar. The tensile moduli ( Figure 3 C) from the linear slope of 0%–5% strain are 725 ± 196 kPa, 864 ± 334 kPa, and 2248 ± 371 kPa in circumferential, radial, and vertical directions, respectively, indicating distinctive mechanical anisotropy perpendicular to/along the fiber axis. When large extension >10% is reached, the curves in circumferential and radial directions experience obvious uplift in stress, indicating strain-hardening. In contrast, the compressive modulus in the vertical direction is much smaller (17.7 ± 9.7 kPa). Therefore, the vertical tensile modulus of natural remora lip tissue is 2- to 5-fold greater than the circumferential and radial modulus and two orders of magnitude greater than the vertical compressive modulus. Compared with the moduli of natural soft tissues reported previously, the radial and circumferential tensile modulus of remora disc lip tissue is comparable with the fish skin and muscle tissue,whereas the vertical compressive modulus is comparable with that of other sucker tissues, such as toe pad of tree frogs (E ∼ 4–25 kPa),octopus sucker (E ∼ 10 kPa),grasshopper (E ∼ 20–65 kPa),and tube feet discs of sea stars (E ∼ 6.0 kPa) and sea urchins (E ∼ 8.1 kPa).

Adhesion Performance of the Biomimetic Suction Disc

a = 200 μm) surfaces were chosen as substrates. When an external preload was exerted on the suction disc, the disc makes contact with the substrate to form a seal and the water inside the disc is discharged to cause a pressure difference. As shown in a = 200 μm) that is comparable with that of the adhesive disc made of pure Ecoflex silicone ( a = 200 μm). The pull-off stress σ (σ = F/A, where A represents the area of the disc pad) can be calculated. The biomimetic composite disc possesses σ ranging from 50 to 57 kPa on smooth surfaces to 47 to 57 kPa on the R a = 200 μm rough surfaces both with 1–20 N preload, compared with 50 to 80 kPa for commercial suction cups on smooth surfaces. The suction pad of the biological remora could achieve a pull-off force of 79.0 N and stress of 46.6 kPa on sharkskin surface (R a ∼ 120 μm), 36 Beckert M.

Flammang B.E.

Anderson E.J.

Nadler J.H. Theoretical and computational fluid dynamics of an attached remora (Echeneis naucrates). Figure 4 Underwater Attachment Performance of the Biomimetic Suction Discs Show full caption (A) Representative force-time profiles of the synthetic discs made from Ecoflex, MoldStar, and nylon fiber/silicone composite with a preload of 20 N on smooth and rough (R a = 200 μm) surfaces underwater. (B and C) Pull-off force as a function of preload force (1, 5, 10, 15, and 20 N) on smooth (B) and rough (C) surfaces (n = 5). Error bars denote ±SD. (D) Pull-off force or maximum detachment force of the synthetic disc from (A). ***p ≤ 0.001; ns, not significant. p values were determined by Student's t test. (E) Adhesion enhancement of composite disc with 1–20 N preload on smooth and R a = 200 μm substrate compared with pure silicone disc. (F) Attachment time of the suckers under a constant 50-N load on a R a = 50 μm substrate (n = 5). Error bars denote ±SD. The biomimetic composite combines the mechanical anisotropy and the viscoelastic behavior, which is hypothesized to bring forth improved adhesion performance. Here, two typical isotropic silicones for making suction discs are chosen as controls, the pure soft matrix rubber (Ecoflex silicone, E ∼ 55 kPa) and another rubber (MoldStar silicone, E ∼ 662 kPa). The pull-off experiments ( Figure S9 ) are conducted under different applied preload forces (1, 5, 10, 15, and 20 N) underwater, and representative change of normal force during the attachment and detachment is shown in Figure 4 A. Smooth and rough (R= 200 μm) surfaces were chosen as substrates. When an external preload was exerted on the suction disc, the disc makes contact with the substrate to form a seal and the water inside the disc is discharged to cause a pressure difference. As shown in Figure S10 , when the disc has a lower vertical compressive modulus, it can follow the contours of a substrate to form a better seal and maintain the pressure differential. During the detachment process, the disc internal volume and the pressure differential increase ( Figure S11A ). The edge of the disc deformed toward the center of the disc, caving inward, eventually causing the attachment to fail, and both the force and the pressure differential drop to zero. The fibrous structure embedded in the composite disc delays the process of caving inward, restrains the deformation caused by pull-off force while maintaining a good seal with the substrate, and eventually results in a significantly higher pressure differential and higher pull-off force ( Figures 4 B and 4C; Videos S2 and S3 ). The biomimetic composite disc generates a considerable pull-off force in the ambient underwater environment, measuring up to 404 N on the smooth surface and 402 N on the rough surface. Compared with the two pure silicone suction discs, the biomimetic composite disc shows greater pull-off force on both surfaces, whereas the soft silicone (Ecoflex) suction disc shows smaller pull-off force on both surfaces, with a non-significant difference in pull-off force between the two surfaces (302 N and 301 N on the smooth and rough surface, respectively). The pull-off force of the stiffer silicone (MoldStar) suction disc is reduced dramatically from smooth (417 N) to rough (234 N) surfaces. Ecoflex has a higher surface roughness than MoldStar ( Figure S12 ), which is supposed to decrease attachment performance of a suction disc made of Ecoflex, but on the other hand the softer Ecoflex-based suction disc can deform more easily. The composite suction disc can maintain the highest pressure differential, thus resulting in better pull-off performance ( Figures 4 D and S11 B). We observe maximum adhesion enhancement of 62.5% using the fiber-reinforced adhesive disc on the rough surface (R= 200 μm) that is comparable with that of the adhesive disc made of pure Ecoflex silicone ( Figure 4 E). Moreover, a preload of 1 N is sufficient for the composite disc to achieve robust, high pull-off force (∼333 N) even on the rough surface (R= 200 μm). The pull-off stress σ (σ = F/A, where A represents the area of the disc pad) can be calculated. The biomimetic composite disc possesses σ ranging from 50 to 57 kPa on smooth surfaces to 47 to 57 kPa on the R= 200 μm rough surfaces both with 1–20 N preload, compared with 50 to 80 kPa for commercial suction cups on smooth surfaces. The suction pad of the biological remora could achieve a pull-off force of 79.0 N and stress of 46.6 kPa on sharkskin surface (R∼ 120 μm),and our biomimetic sucker achieves a force value close to these biological data. In addition, the sucker can repeat at least 100 cycles without a significant decrease in the pull-off force ( Figure S13 ).

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a = 50 μm) surface underwater. The underwater attachment time extended from ∼6 min (pure silicone suction disc) to ∼26 min (biomimetic composite suction disc), generating ∼340% improvement, while the attachment time of the stiffer suction cup is only ∼4 min. The biomimetic sucker is also proved to improve the attachment time (generating a ∼270% increase) on dry, smooth substrates ( During hitchhiking, remoras need to maintain attachment on a wide range of surfaces. Therefore, a sucker needs to be capable of maintaining robust and strong adhesion on rough surfaces under external load. Figure 4 F shows the role of vertical fibers in maintaining the attachment on a rough (R= 50 μm) surface underwater. The underwater attachment time extended from ∼6 min (pure silicone suction disc) to ∼26 min (biomimetic composite suction disc), generating ∼340% improvement, while the attachment time of the stiffer suction cup is only ∼4 min. The biomimetic sucker is also proved to improve the attachment time (generating a ∼270% increase) on dry, smooth substrates ( Figure S14 ). Concerning the suction on dry and rough substrates, the biomimetic suckers need to be connected to a vacuum pump to ensure initial sealing. Our results suggest that the biomimetic sucker is better at maintaining attachment due to the tensile creep resistance of the composite.

a = 200 μm) substrates underwater. However, limited by the equipment and fiber properties, the maximum fiber flocking density in this work is ∼8%. To verify the effect of fiber density in the composite, we have made composites with varied fiber densities and their corresponding suction discs. The results ( Figure S15 ) show that higher fiber density results in higher vertical tensile modulus of the composite and higher pull-off forces of the suction disc on both smooth and rough (R= 200 μm) substrates underwater. However, limited by the equipment and fiber properties, the maximum fiber flocking density in this work is ∼8%.

Figure 5 Demonstration of the Circular Suction Disc, Biomimetic Sucker, and Actuators Show full caption (A) Fiber-reinforced circular suction disc as gripper lifting various objects such as 75-g raw egg, 76-g alive crayfish, 216-g orange, 130-g bottle, 280-g volleyball, and 153-g plastic bag. Scale bar, 10 cm. (B) Biomimetic sucker lifted a 5.5-kg watermelon and was attached to the wall with a load of 4 kg of water in a moist environment. Scale bar, 10 cm. (C) Schematic diagrams of rubber block, anisotropic composite blocks, and structures of actuators. (D) In these demonstrations, the inside vertical fibers limit the extension of the rubber matrix and result in special elongation and bending. Scale bar, 20 mm. For wider applications, we consider the fibrous structure embedded in materials as an effective strategy for improving pull-off force irrespective of the geometry of the suction disc. The vertically aligned fiber composite is incorporated into circular suction cups, providing over 50% pull-off force improvement ( Figure S16 ). We also connect the fiber-reinforced sucker with tubing and a vacuum pump as a gripping system, which shows abilities to lift a wide range of objects with various sizes and shapes ( Figure 5 A). This fiber-reinforced sucker system possesses high surface conformability while simultaneously maintaining high pull-off force due to the deformability in radial and circumferential directions and high tensile vertical stiffness. While the fiber-reinforced sucker can easily lift the 280-g volleyball, the common silicone sucker cannot, thus demonstrating the superior suction adhesion performance of our fiber-reinforced composite sucker. Also, the biomimetic composite suction disc was used to suspend heavy and irregular objects such as a watermelon and 4 kg of bottled water in a moist environment to demonstrate the functionality ( Figure 5 B).

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More interestingly, such strategies of fabricating composite materials with defined fiber orientation for morphology anisotropy can be applied in soft pneumatic actuators, i.e., for controlled deformation and “smart” behaviors. Because the fibers will limit the axial tensile deformation, by placing the fibers in the middle or at both ends, the soft pneumatic actuator can be elongated at a specific position without fiber; bending and asymmetric bending can be achieved by placing the fibers on one side or on different sides ( Figures 5 C and 5D). The quantitative data and process are shown in Figure S17 and Video S4 . These motions in actuators may enrich the locomotion of future soft robotics across scales.