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The co‐effect of microstructures and mucus on the adhesion of abalone from a mechanical perspective

2021; Institution of Engineering and Technology; Volume: 7; Issue: 4 Linguagem: Inglês

10.1049/bsb2.12024

2405-4518

Jing Li, Chuandong Ma, Jun Liu, Xiangwei Dong, Jianlin Liu,

Force Microscopy Techniques and Applications

Biosurface and BiotribologyVolume 7, Issue 4 p. 180-186 ORIGINAL RESEARCH PAPEROpen Access The co-effect of microstructures and mucus on the adhesion of abalone from a mechanical perspective Jing Li, Corresponding Author Jing Li lijing85@upc.edu.cn orcid.org/0000-0001-8735-9427 College of Mechanical and Electrical Engineering, China University of Petroleum (East China), Qingdao, China Correspondence Jing Li, College of Mechanical and Electrical Engineering, China University of Petroleum (East China), Qingdao 266580, China. Email: lijing85@upc.edu.cnSearch for more papers by this authorChuandong Ma, Chuandong Ma College of Mechanical and Electrical Engineering, China University of Petroleum (East China), Qingdao, ChinaSearch for more papers by this authorJun Liu, Jun Liu College of Mechanical and Electrical Engineering, China University of Petroleum (East China), Qingdao, ChinaSearch for more papers by this authorXiangwei Dong, Xiangwei Dong College of Mechanical and Electrical Engineering, China University of Petroleum (East China), Qingdao, ChinaSearch for more papers by this authorJianlin Liu, Jianlin Liu College of Pipeline and Civil Engineering, China University of Petroleum (East China), Qingdao, ChinaSearch for more papers by this author Jing Li, Corresponding Author Jing Li lijing85@upc.edu.cn orcid.org/0000-0001-8735-9427 College of Mechanical and Electrical Engineering, China University of Petroleum (East China), Qingdao, China Correspondence Jing Li, College of Mechanical and Electrical Engineering, China University of Petroleum (East China), Qingdao 266580, China. Email: lijing85@upc.edu.cnSearch for more papers by this authorChuandong Ma, Chuandong Ma College of Mechanical and Electrical Engineering, China University of Petroleum (East China), Qingdao, ChinaSearch for more papers by this authorJun Liu, Jun Liu College of Mechanical and Electrical Engineering, China University of Petroleum (East China), Qingdao, ChinaSearch for more papers by this authorXiangwei Dong, Xiangwei Dong College of Mechanical and Electrical Engineering, China University of Petroleum (East China), Qingdao, ChinaSearch for more papers by this authorJianlin Liu, Jianlin Liu College of Pipeline and Civil Engineering, China University of Petroleum (East China), Qingdao, ChinaSearch for more papers by this author First published: 23 August 2021 https://doi.org/10.1049/bsb2.12024AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Abstract Reliable and reversible adhesion underwater is challenging due to the water molecules and weak layers of contaminants at the contact interface, which requires to deepen the understanding of wet adhesion of biological surfaces. Herein, the co-effect of microstructures and mucus of abalone foot on wet adhesion is investigated from both experimental and theoretical perspectives. The morphologies, adhesion force and coefficient of friction indicate that the mucus in adhesion zone is crucial for successful attachment of abalone based on capillary forces and viscous forces, and the mucus in non-adhesion zone with lower adhesion force and friction coefficient may behave as a lubricant for the locomotion. The theoretical calculation manifests that the microstructures may help abalone to form multiple liquid bridges with the secreted mucus, and significantly increase the wet adhesion force of abalone. These findings will bring profound views into the underlying mechanisms of biological surface adhesion. 1 INTRODUCTION Under aqueous conditions, the water molecule will enter the adhesive interface and form a thin hydration film [1-3], which may reduce the contact area, or generate hydration, swelling and even degradation of the adhesive molecule, resulting in rapid loss of the adhesion between the two contact surfaces. Therefore, an adhesive, a mechanical interlock, van der Waals forces and other common methods of adhesion are limited in water. Developing intelligent underwater adhesion surfaces has proven to be a challenging problem in the field of engineering. Many marine animals possess extremely strong adhesion ability underwater, which has attracted great attention and research interests of many scholars. In nature, marine animals often adopt the strategies of gluing (chemical bonding) and suction to fulfil underwater adhesion. For example, mussels form permanent adhesion in the turbulent ocean environment by producing quick-acting protein-based glues [4, 5]. Barnacles utilise an adhesive multi-protein complex (barnacle cement), to accomplish permanent attachment to various surfaces [6, 7]. Sandcastle worms utilise self-made adhesive to bond gravels and biomineral particles to form a strong tubular protective cover [8, 9]. In addition, organisms such as algal cells, marine flatworms, and bacterial biofilms utilise amyloid structures to achieve interfacial adhesion in aqueous environment [10-12]. Suction is another common attachment mechanism for marine animals. For instance, octopus, clingfish, remora fish and other temporary adhesion organisms mainly rely on the effect of sucker structure to achieve underwater adhesion [13-17]. In addition to the adhesion of above mentioned animals, abalone uses its flexible pedal foot, covered with a large number of micrometre-scaled fibres, to cling and adhere solidly to rocks at sublittoral depths. The normal adhesion force mainly originates from the pedal suction pressure, van der Waals force and capillary force, which can reach 200 or 300 times of its body weight [18]. When the abalone is pulled off from the substrate, it leaves a deposited mucus layer, which consists of a large part of water and sugar polymers [19]. In addition to the extremely strong adhesion, abalone can also leave the substrate and move around independently, in which case, the secreted mucus also plays an important role. A similar phenomenon is observed in terrestrial gastropods, such as snails and slugs [20-25]. Furthermore, Lin et al. [26] used the atomic force microscope (AFM) to measure the adhesion force of a single seta distributed on the foot, and found that the main sources of microscopic adhesion are van der Waals force and capillary force. Besides, Tadmor et al. [27] designed a method to measure the adhesion of solid–liquid of adhesion forces, and proposed mathematical equations for calculating the London–van der Waals (vdW) interaction energies between macroscopic objects [28]. However, the combined role of the mucus and the micrometre-scaled fibres on the foot needs to be further explored, and the mechanical properties of the mucus secreted are still unknown. The motivation of the present work is therefore to investigate how this complex fluid affects the interaction between the abalone and a solid substrate. First, we introduce the experiments of measuring the adhesion and microstructures of mucus collected in adhesion and non-adhesion zones, respectively. Next, we analyse the effect of microstructures on wet adhesion from a theoretical perspective. It is anticipated that this study will help us re-recognise the adhesion phenomena and provide some inspirations for bioinspired wet adhesive surfaces. 2 MATERIALS AND METHODS 2.1 Sample preparation The abalones (Haliotis discus hanna, 3 years old, 7 cm in length) used in the experiments are cultured in a transparent cuboid aquarium with the volume of 80 × 60 × 100 cm3 at 18 ± 1 °C for at least three days to acclimate to the laboratory environment. The abalone is kept physically stimulated for 30 min before being taken out of the aquarium. Then, the abalone is peeled off the substrate after the water around the body is removed by filter paper, and two different kinds of mucus can be collected on the substrate. One is the pale yellow colloidal mucus secreted in the adhesion area in the middle part of the pedal, hereinafter referred to as the adhesion area mucus. The other is a kind of transparent mucus collected from the tentacle part around the skirt, hereinafter referred to as the non-adhesion area mucus. 2.2 Characterisation Morphologies of lyophilised mucus samples and pedal foot are observed using a scanning electronic microscope (SEM, COXEM EM-30 Plus). The foot tissue is sectioned from its body without changing the surface topography (5 × 5 × 3 mm3). Then, the samples are placed in ultrapure water and cleaned with an ultrasonic cleaner (kq-300de, Kunshan Ultrasonic Instrument Co., Ltd.) for 5 min. After being kept in 4% formaldehyde for at least 12 h, the samples are dehydrated successively with 30%, 50%, 70%, 85%, 90%, 100% ethanol for 15 min each time. Finally, the samples are pre-cooled in a vacuum freeze dryer (BK-FD10S, Shandong Brocade Bio-Industry Co., Ltd.) under −60 °C for 4 h, and then dried at a vacuum of less than 10 Pa for at least 8 h. Both the adhesion area mucus and non-adhesion area mucus are also freeze-dried to obtain a lyophilised observation sample. Before observation, all the samples are sputtered with a thin layer of gold to enhance the electron conductivity. 2.3 Adhesion measurements The normal adhesion force is measured with a self-made adhesion tester between a bearing steels probe (5 mm in diameter) and a flat substrate [29]. The substrate is a sheet of soft silica gel with dimensions of 30 × 30 × 2 mm3, and the Young's modulus is E = 0.47 MPa, which is measured by a universal testing machine (UTM–1432, Cheng De Jin Jian Testing Instrument Co. Ltd). First, 3 μl of mucus is dripped onto the substrate. Then, the probe approaches the substrate and a preload of 10 mN is applied. After the approaching, there is a 10 s pause at this position to achieve stability of the system, and the separation is performed at a speed of 57 μm·s−1. The shear adhesion of the mucus is conducted with a micro friction and wear tester (WTM-2E, Lanzhou Zhongke Kaihua Technology Development Co., Ltd). The counterbody used here is a ball, which is the same with the probe used in the normal adhesion measurements. The platen is rotated at 300 r/min with the radius of 5 mm, and the normal applied load is about 0.2 N. To measure the friction coefficient of the adhesion area mucus in situ, a piece of fresh abalone foot is cut off along the attachment muscle as the substrate. In order to compare the adhesion area mucus, the abalone foot cut off along the attachment muscle is first cleaned with ultrasound for 40 min to remove the adhesive mucus, and evenly smeared with non-adhesion area mucus, then the procedure of measuring the friction coefficient is repeated. 3 RESULTS AND DISCUSSION 3.1 The role of mucus In order to investigate the effect of mucus, the abalone foot is first cut off along the attachment muscle, and cleaned with ultrasound for 10 to 40 min to remove the mucus. Figure 1a–d shows the SEM micrographs of the foot with different ultrasonic cleaning times, covered with a large number of micrometre-scaled fibres. It can be observed that the surface is covered with mucus when the abalone foot without ultrasonic cleaning is examined (Figure 1a). The amount of mucus decreases with increasing the ultrasonic cleaning time, and there is some flaky mucus on the fibres (Figure 1b,c). The fibres become clearer when most of the mucus is removed (Figure 1d). The abundant secreted mucus indicates that the mucus may act in synergy with the micrometre-scaled fibres at the adhesion interface. Furthermore, the morphology of the mucus is observed as shown in Figure 2. On a macroscopic view, the mucus in adhesion zone is viscoelastic, while the mucus in non-adhesion zone is a liquid with good fluidity and ductility. From the microscopic view, the former is loose and porous composed of many fine flakes (Figure 2a), the structure of which may be prone to adsorb and remove the moisture, thus creating a better adhesion environment for abalone. Compared with the mucus in adhesion zone, there are more flake structures of the mucus in non-adhesion zone (Figure 2b), and the overlapping part of the flake structure is connected by fibrous mucus, which may easily realise the slip between the flake mucus and help reduce the crawling resistance of abalone. Therefore, the two kinds of mucus may play different roles in adhesion and locomotion, respectively. In addition, the morphology difference of the mucus may be related to the chemical composition, for example concentration of proteins [20], which will be systematically investigated in future studies. FIGURE 1Open in figure viewerPowerPoint Scanning electronic microscope micrographs of the abalone foot for different cleaning time. (a) 0 min; (b) 10 min; (c) 20 min; (d) 40 min FIGURE 2Open in figure viewerPowerPoint Scanning electronic microscope micrographs of abalone mucus. (a and b) Mucus in adhesion zone; (c and d) mucus in non-adhesion zone Subsequently, adhesion measurements are conducted as shown in Figure 3 to investigate the different roles of both kinds of mucus from a mechanical perspective. Figure 3a exhibits representative force-distance curves of mucus on a silica gel sheet. The maximum wet adhesion of mucus occurs at the position where the probe and the substrate have just separated. With further separation, the adhesive force of the mucus in adhesion zone will rapidly decrease, and reduce to zero when the capillary bridge is broken. While the adhesive force of the mucus in non-adhesion zone decreases gently, and the long force-distance trend is related to good fluidity and ductility of the mucus. Figure 3b shows the maximum adhesion of abalone mucus, water and methylsilicone oil. It can be seen that the maximum adhesion of mucus in adhesion zone is about 3.3 mN, which is twice as large as that of the mucus in non-adhesion zone, nearly 5 and 10 times higher than that of methylsilicone oil and water, respectively. The coefficient of friction (COF) of mucus is measured as illustrated in Figure 3c. The curve of the mucus in adhesion zone shows a higher friction coefficient of 0.13, and the mucus in non-adhesion zone has a lower friction with a coefficient of 0.07. The results indicate that the mucus in adhesion zone plays a crucial role in attachment of abalone based on capillary forces and viscous forces through a liquid bridge. While the mucus in non-adhesion zone with lower adhesion force and COF may behave as a lubricant for the foot when an abalone moves. The results are essentially in agreement with the morphologies of the mucus. It should be noticed that the small value of COF may indicate that the adhesion force of abalone in the shear direction is lower than that in the normal direction, which is in agreement with our previous experimental study on the adhesion measurements of the whole abalone [18]. Besides, the low COF may explain why peeling of an abalone usually needs a force close to the shearing direction in reality. FIGURE 3Open in figure viewerPowerPoint (a) Force-displacement curves; (b) adhesion forces and (c) coefficients of friction for different abalone mucus 3.2 Theoretical analysis Based on the experimental data, there is one question below: How does the adhesion force depend on both the microstructure and mucus in adhesion zone? However, it is difficult to observe the microstructure of adhesion interface of abalone in situ. Thus, theoretical models and analysis on the adhesion are further discussed. One generally theoretical model is established as schematically shown in Figure 4a. If there is a small amount of liquid between the two surfaces, they may contact through n small individual bridges providing that microstructures are considered. It is assumed that the bridges are independent of each other, and the total volume of n small bridges is equal to the volume of the single large bridge V shown in Figure 4b. For each small liquid bridge, the ordinary differential equations are given as { d x d s = cos ϕ d y d s = sin ϕ d ϕ d s = Δ p γ − sin ϕ x , (1)where x and y are the co-ordinates of the liquid bridge, s is the arc length of the liquid profile, and ϕ is the angle between the local tangent of liquid surface and the horizontal axis. γ is the liquid surface tension, and Δp is the pressure difference. While pulling the liquid bridge in the normal direction, the corresponding boundary conditions can be established based on two contact states, that is, radius controlled state and angle controlled state. The boundary conditions for the two states are written as Equations (2) and (3), respectively. { x 1 = R p , y 1 = 0 , ϕ = θ ∗ y 2 = h , ϕ = θ 2 V = 1 n ∫ 0 y 2 π x 2 d y , (2) { x 1 = R 0 , y 1 = 0 , ϕ 1 = π − θ 1 y 2 = h , ϕ 2 = θ 2 V = 1 n ∫ 0 y 2 π x 2 d y , (3)where h is the separation height between the upper surface and the lower surface. Rp is the radius of a single microstructure, and R0 is the radius of the liquid bridge. θ1 and θ2 are the contact angles of the two surfaces, respectively. When the separation height is small, it is in the radius controlled state, and the periphery of the liquid is pinned at the surface of the microstructure at the angle θ*, which can be calculated according to the separation height. The capillary force of a single small liquid bridge along the normal direction can be given as F c 1 = π γ ( − x 1 2 Δ p γ + 2 x 1 sin θ ) , (4)where θ is the angle between the microstructure and the liquid, and the total capillary force of n liquid bridges is F = n F c 1 . (5) FIGURE 4Open in figure viewerPowerPoint Schematic of the contact model. (a) n small independent liquid bridges; (b) a large single liquid bridge For calculation, the two surfaces are pulled apart for a given volume of methylsilicone oil with 3 μl, and the contact angle θ is 10°, which are measured in the experiments. The total force varies with the number of bridges n as displayed in Figure 5, using γ = 21.1 mN/m for the methylsilicone oil–air interface, the wetting property of which is the same as that of mucus. The calculation results show that the total capillary force of n small liquid bridges is larger than that of a single large liquid bridge with the same total liquid volume. In addition, the contact area may also affect the capillary force. In calculation, if the effect of gravity on the shape of the liquid bridge is ignored for traces of liquid, the liquid bridge scales in the direction of length, width and height for different volumes. The number of the bridges and the volume will change at the same time to ensure that the total area of the liquid bridges projected onto the substrate is the same. Figure 5b exhibits the adhesion forces with different numbers and total volumes of small liquid bridges when the total area of the bridges projected onto the substrate is the same. The results indicate that subdividing one liquid bridge into multiple smaller ones between two surfaces can produce a larger capillary force with the same contact area and less volume of the liquid. It means that wet adhesion organisms can reduce mucus secretion and energy loss during adhesion, which is obviously very beneficial. FIGURE 5Open in figure viewerPowerPoint Capillary forces of multiple liquid bridges. (a) With a given liquid volume; (b) with the same contact area In contrast, if an abalone adheres to a surface under the water with too much water, or it secretes and spreads excessive mucus, there will be enough liquid between the two surfaces, and the liquid will fill the microchannels and cover the surface with a layer of water film. Then, one large liquid bridge may exist and microstructures are completely immersed in the liquid (as shown in Figure 4b). The microstructures can be regarded as a part of the whole liquid bridge, thus the model and ordinary differential equations are the same as the two smooth surfaces [29]. The surface profile of the liquid bridge has smaller curvature with larger liquid volume, which will result in smaller axial force of the liquid surface tension, thus reducing the capillary force (as shown in Figure 6). The results, in accordance with the Qian and Gao's calculation [30], indicate that too much liquid will reduce the adhesion of wet adhesion organisms. In addition, the results are in accordance with typical natural bioadhesion. For instance, because the channels between the protuberant polygonal epithelial cells can facilitate the spreading of mucus and removing of excess liquid on the surface, a liquid bridge is formed between the contact element and the substrates, tree frogs are able to flexibly climb on wet trees by capillarity adhesion [31]. While the abalones can remove water by spreading of their feet (the process as shown in Figure 7), which will help form solid wet adhesion underwater. FIGURE 6Open in figure viewerPowerPoint Capillary forces for different volumes of the microstructures FIGURE 7Open in figure viewerPowerPoint (a) The spreading process of the abalone foot; (b) the process of removing bubbles Macroscopically, the abalone foot is an elliptical structure with many folds on its surface. The whole foot will be wrapped into semi-open nuts in order to protect the surface of abalone without contacting any substrate. As shown in Figure 7a, when there is a suitable surface, the wrapped foot will continue to flip out and begin to adhere to the substrate from the centre part, where the folds become smaller and disappear. During the spreading process of the abalone foot, air bubbles will appear during the contact interface as shown in Figure 7b. The abalone will drain the bubbles by spreading the foot, and remove the excessive water at the same time to form pressure difference. Then, the microstructures may help it to adapt to rough substrates, and form multiple liquid bridges with the secreted mucus, where the multiple liquid bridges will increase the capillary force. Finally, the abalone adheres solidly to the surface. 4 CONCLUSIONS In conclusion, the co-effect of microstructures and mucus of the abalone foot on the wet adhesion has been investigated from both experimental and theoretical perspectives. The viscoelastic mucus in adhesion zone is loose and porous composed of many fine flakes, which has larger adhesion force and COF. There are more flake structures of the mucus liquid in non-adhesion zone, and the adhesion force and COF are smaller. The results indicate that the mucus in adhesion zone is crucial for the successful attachment of abalone based on capillary forces and viscous forces, and the mucus in non-adhesion zone may behave as a lubricant for the locomotion. Besides, the low COF indicates lower shear adhesion, which is accordance with the experimental study of the whole abalone in our previous study. The theoretical calculation manifests that the microstructures will help the abalone to form multiple liquid bridges with the secreted mucus, and the wet adhesion force of the abalone will increase significantly. Although there are several issues that need further consideration, such as the chemical effect of the mucus, the engineering application, we expect these findings help us re-recognise the adhesion phenomena and provide some inspirations for bioinspired multiscaled wet adhesive surfaces. ACKNOWLEDGEMENTS This project was supported by the National Natural Science Foundation of China (51975586, 11672335) and the Fundamental Research Funds for the Central Universities (19CX02018A). Open Research DATA AVAILABILITY STATEMENT The data that support the findings of this study are available from the corresponding author upon reasonable request. REFERENCES 1Zhao, Y.H., et al.: Bio-inspired reversible underwater adhesive. Nat. Commun. 8(1), 2218 (2017) CrossrefPubMedWeb of Science®Google Scholar 2Hofman, A.H., et al.: Bioinspired underwater adhesives by using the supramolecular toolbox. Adv. Mater. 30(19), 1704640 (2018) Wiley Online LibraryPubMedWeb of Science®Google Scholar 3Ditsche, P., Summers, A.P.: Aquatic versus terrestrial attachment: water makes a difference. Beilstein. J. Nanotechnol. 5, 2424– 2439 (2014) CrossrefPubMedWeb of Science®Google Scholar 4Waite, J.H.: Mussel adhesion – essential footwork. J. Exp. 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