Research on the drag reduction and vibration attenuation performances of the fish’s surface mucus film

doi:10.21203/rs.3.rs-4272590/v1

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Research on the drag reduction and vibration attenuation performances of the fish’s surface mucus film

https://doi.org/10.21203/rs.3.rs-4272590/v1

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This study is the inaugural investigation into the drag reduction and vibration attenuation performance of mucus films naturally present on fish surfaces, leveraging nanomechanical systems for a comprehensive understanding. The mucus was collected from healthy Asian carps. Four testing groups were the fish scale surfaces adsorbed musus for 1 min, 5 min, 10 min and 30 min, respectively. Bare scale was used as a control. The mechanical and lubrication properties of the mucus film were tested using a nano scratch/indentation tester. And the vibration attenuation performance of the film was examined by a self-developed vibration excitation device. Results show that the mucus film and the surface of fish scales combine through electrostatic interactions, ultimately forming a smooth inner layer. As the adsorption time progresses, additional proteins gradually accumulate, forming a thicker outer layer. Notably, the inner layer possesses a significant lubrication effect, effectively preventing friction and wear caused by underwater sand and gravel. Furthermore, the outer layer exhibits an excellent vibration attenuation effect, assisting Asian carp in overcoming the resistance caused by turbulence and enhancing swimming speed.

Fish

mucus film

drag reduction

vibration attenuation

adsorption

Underwater vehicles are currently the indispensable equipment for executing underwater missions, playing a pivotal role in the deep sea exploring[1]. During these exploratory endeavors, the vehicles encounter a significant obstacle: the impact of water flow on their surface results in the formation of a turbulent boundary layer, which not only causes vibrations on the vehicle's surface but also increases resistance[2]. Consequently, this leads to a notable decrement in both the speed and endurance of the underwater vehicles, thereby substantially compromising their exploratory capabilities. This obstacle not only hampers the efficiency of the vehicles but also poses a considerable challenge to the field of underwater exploration. Therefore, mitigating surface drag emerges as a pressing necessity, underscoring the paramount importance of surface drag reduction as a critical challenge that the field currently faces[3].

The ability of fish to swim flexibly and quickly has always been an ideal goal pursued by underwater vehicles[4]. In recent years, revealing the formation mechanism of the drag reduction function in fish's surface and designing biomimetic drag reduction technology have been hot research topics to improve the navigation ability of underwater vehicles. Researchers have found that the unique non-smooth skin of fish can suppress turbulent boundary layers. Therefore, they are committed to studying the characteristic structure of this non-smooth skin and have developed biomimetic drag reduction surfaces mainly consisting of groove structure, mastoid structure, and shield scale structure[5-7]. Unfortunately, when the biomimetic surface comes into direct contact with sand and gravel in water, its micro texture is severely worn, and the drag reduction effect is greatly reduced, sometimes even leading to an increase in resistance.

In addition to its unique surface structure, the fish body can also secrete mucus through the goblet cells on the surface, which can effectively adsorb onto the scale and form a stable adsorption film [8, 9]. Research has shown this film separates the fish body from the turbulent boundary layer and reduces the turbulent friction resistance by about 60%[10]. Theoretically, the drag reduction ability of the fish surface comes from the effective coordination of its unique surface structure and the mucus film. However, obtaining the thin film structure of the mucus film remains challenging due to its nanoscale thickness and the strong adsorption forces of mucus molecules. Conventional morphology testing methods, such as electron microscopy and atomic force microscopy, have proven insufficient in elucidating its intricate structure. Consequently, despite some researchers discovering its remarkable drag reduction characteristics, the underlying mechanism remains elusive.

In this study, we employed nanoindentation mechanical testing methods for the initial indirect exploration of the adsorption and film-forming characteristics of fish mucus in vitro. Meanwhile, the lubricating properties performance of the mucus film were tested using nano-scratch technique. And the vibration attenuation performance of the film was examined by a self-developed vibration excitation device. Considering that the lubricating properties of sthe mucus film are closely associated with its adhesion to substrates, the adhesion force between the mucus film and the fish scale was measured using Atomic Force Microscopy.

2.1. Sample preparation

The fish used in this study are Asian carp, which are highly adaptable and widely distributed around the world[11]. All fish are purchased from aquiculture farms. The collection process of the samples complies with the ethical standards of the Chinese Ethics Society.

The mucus was collected using an unstimulated method [12], and to avoid individual differences, the pre-sample cam from a mixture of ten fish. After centrifugation at 2000 g for 30 minutes, the supernatant was taken to obtain the final mucus sample. In order to avoid protein denaturation, the collected samples were tested within 2 hours. The fish scales of Asian carp were selected as the adsorption substrate for mucus. To prevent dehydration, the collected scales were stored in physiological saline (0-4 ℃) for later use.

Finally, the adsorption time of the mucus on the scale surface was 1, 5, 10, and 30 minutes, respectively. And the samples adsorbed different mucus film were named SAF1, SAF2, SAF3, and SAF4 in order.

2.2. Film forming performance tests by mechanical properties characterization

As previously mentioned, obtaining the morphological structure of fish mucus films through conventional testing methods is challenging. Therefore, in this study, we indirectly characterized the film-forming performance of fish mucus using the nanomechanical systems.

Penetration force was measured at the continuous stiffness measurement (CSM) mode [13] using a nano-indenter (NanoIndenter G200, keysight, USA). A Berkovich diamond tip with a radius of 20 nm was used. All tests were conducted at a constant strain rate (0.05/s) and a limited thermal drift (< 0.5 nm/s) with a frequency of 45 Hz. The maximum indentation depth was 500 nm.

Adhesion force was measured using an Atomic Force Microscopy (AFM) (CSPM5500, Being Nano-Instruments, China) . It is known that AFM is an ideal tool to measure the interaction forces between the tip and a surface [14]. In this study, a silicon dioxide tip with a nominal radius of 2 μm was used. The adhesion force between bare tip and bare scale surface was measured as a control. Then, the tip was incubated in the previously collected mucus sample for 1~30 min to obtain a tip coated with different mucus film. The adhesion forces of the modified tip on the bare/adsorbed fish scale surface were measured to asses the adhesion performance of different interfaces.

2.3. Lubrication performance tests

To investigate the film lubrication behavior on the fish scale surface, unidirectional nano-scratch tests at constant load mode were conducted at room temperature using a nano-scratch tester (G200, keysight, USA). A conical diamond tip with a radius of 10 μm was used, and the applied normal load was 20 mN. The scratch length was 50 μm, and the scratching speed was 5 µm/s.

2.4. Zeta potential tests

The adsorption of natural protein film is mostly driven by electrostatic interaction between proteins and adsorption surface, and the zeta potential was a significant parameter to characterize this process [15]. In this study, the zeta potentials of both the bare fish scale and the incubated fish scale were measured by Zetasizer (BeNano, Baite, China) at room temperature. For the detailed method of sample preparation, see reference [16].

2.5. Vibration attenuation performance tests

The vibration induced by turbulence poses additional resistive forces, thus weakening the navigational capabilities of underwater vehicles [17, 18]. The remarkable high-speed swimming capabilities of fish suggest the possibility of a damping mechanism within their mucus film. To test this hypothesis, we conducted high g-value impact tests on samples with varying adsorption treatments by a self-developed vibration excitation device (Figure 1), all under identical excitation energy[19]. Acceleration signals were measured across various g-value levels and pulse widths. These signals were then digitally integrated according to standard protocol to determine the velocity changes of the mucus films throughout the impact process. Furthermore, the energy changes during the impact process were calculated to assess the vibration attenuation properties of the mucus films.

3.1 Mechanical properties

As detailed in Table 1, The relationship between the penetration force and the adsorption time of the fish mucus film was investigated using a nano-scratch tester. As shown in the Figure. 2 , the penetration forces of the mucus film follow the sequence of SAF4 > SAF3 > SAF2> SAF1. And its thickness exhibits a consistent trend, upon increasing the adsorption time, the mucus film thickness progressively increases from 27.5nm to 105.5nm (Table 1).

The results, clearly demonstrate an upward tendency in the penetration force required to penetrate the mucus film as the adsorption time increases. This trend suggests that the mucus film becomes more difficult to penetrate as proteins gradually accumulate on its surface over time. To ascertain the statistical significance of the observed differences in penetration forces across various adsorption times, we subjected the nano-scratch test data to rigorous statistical analysis. Both One-way ANOVA and paired t-tests were employed to evaluate the significance of variations in penetration forces and film thickness among the different groups. The statistical tests revealed a significant difference (P < 0.05) in both penetration forces and film thickness between the groups treated with differing adsorption times. This finding underscores that as adsorption time increases, both the thickness of the mucus film and its resistance to penetration grow significantly.

Table 1 Thickness of the mucus film with different adsorption time.

Saliva sample	SAF1	SAF2	SAF3	SAF4
Thickness/nm	27.5±3.8	53.2±4.9	92.4±10.2	105.5±12.6

As depicted in Figure 3, the adhesion force exerted by the mucus film on a bare fish scale (MF-BF) was the strongest, measuring approximately 1380 nN. This high adhesion force suggests a strong interaction between the mucus film and the bare fish scale, likely due to the specific biochemical properties of the mucus that facilitate adhesion. When the mucus film adhered to another mucus film (MF-MF), the adhesion force decreased to 750 nN. This reduction could be attributed to the similar biochemical composition of the interacting surfaces, which might have resulted in a lesser adhesive force compared to the interaction with a dissimilar surface like the bare fish scale [16]. Nevertheless, the adhesion force between mucus films was still higher than that between a bare tip and a bare scale, which was approximately 341 nN. This finding implies that the mucus film possesses inherent adhesive properties that enhance its sticking ability, even when interacting with surfaces of similar composition.

Furthermore, as the adsorption time increased, the adhesion forces between the mucus films became more comparable. This observation suggests that over time, the adhesive properties of the mucus films might undergo changes, possibly due to the interaction with the environment or the rearrangement of mucin molecules within the film. A paired t-test analysis revealed no significant differences between these group pairs (P>0.05), indicating that the adhesion forces between different mucus films tend to converge as time passes. The high adhesion force observed in the mucus film on a bare fish scale could have important implications for the understanding of how fish adhere to various surfaces in their natural habitat. This strong adhesive ability might play a crucial role in their locomotion, feeding, and reproduction behaviors. Future studies could explore the biochemical composition of the mucus film and its interaction with different surfaces to gain a deeper understanding of its adhesive properties. Additionally, the convergence of adhesion forces over time suggests a dynamic nature of the mucus film's adhesive abilities. This finding could have implications for the design of biomimetic adhesives inspired by the mucus film, particularly in terms of their durability and sustained adhesive strength.

3.2 Lubrication performance

The friction coefficients of samples coated with various mucus films are presented in Figure 4. The bare fish scale sample, serving as a control, displays substantial variations in its friction curve and possesses the highest average friction coefficient. This high friction coefficient of the bare scale sample suggests that the absence of a mucus layer leaves the surface more prone to friction, which may explain its wear-prone nature. In contrast, all mucus-treated scale surfaces exhibit lower surface friction coefficients compared to the untreated surface. This reduction in friction is likely due to the lubricating properties of the mucus film, which creates a slippery layer that minimizes direct contact between surfaces. An interesting observation from our study is that the friction-reducing properties of the mucus film decline as adsorption time increases, following the order of SAF4 > SAF3 > SAF2 > SAF1. The nano-lubrication properties exhibited by biofilms are not infrequent occurrences [14], and their presence does not indicate a diminution in lubrication effectiveness.. Instead, the accumulation of adsorbed proteins over time increases the lateral resistance of needle movement.

The experimental results, depicted in Figure 5, further support the beneficial effects of the mucus coating. The mucus-coated samples demonstrate a significant reduction in wear compared to the control group. Obviously, the mucus film acts as a protective layer, reducing friction and wear on the surface. However, our statistical analysis using the paired t-test indicates no significant difference in wear volume among the SF2, SF3, and SF4 groups, suggesting that extending the adsorption time beyond a certain point does not further enhance the wear-reducing effect. This implies that there may be a saturated adsorption time within 5 min for achieving the best lubricating properties of the mucus film.

3.3 Zeta potential

Table 2 presents the zeta potential values measured on the surface of various samples subjected to different adsorption treatments. The control group, consisting of fish scales that did not undergo any adsorption treatment, exhibited a surface potential of -41.2 mV, clearly indicating strong electronegativity. This baseline measurement provides a valuable reference for comparing the effects of subsequent adsorption treatments. Upon adsorbing SF1, a significant increase in the surface zeta potential to -22.5 mV was observed. This shift suggests the occurrence of electrostatic interactions between the mucus and the fish scales. Such interactions are crucial in various biological processes, including adhesion, and their study can lead to a better understanding of the mechanisms involved. Interestingly, the duration of adsorption did not significantly impact the electrostatic effect. As the adsorption time progressed from 1 minute to 30 minutes, the zeta potential of the adsorption surface gradually increased from -22.5 mV to -15.9 mV. This gradual increase indicates that the electrostatic interaction becomes stronger over time, albeit at a slow rate. Thus, the adsorption process might involve multiple stages or mechanisms, with the initial stages having a more significant impact on the zeta potential than the later stages.

Table 2 Zeta potential values on the surface of samples adsorbed with different mucus films

Saliva sample	Control	SAF1	SAF2	SAF3	SAF4
Zeta potential/mV	-41.2±3.3	-22.5±2.5	-18.3±2.9	-16.6±1.2	-15.9±1.6

3.4 Vibration attenuation performance

Figures 6 and 7 clearly depict the variations in acceleration and energy dissipation rates during the impact process, comparing samples before and after the adsorption treatment. Notably, the control group without any mucus film demonstrated the highest peak acceleration accompanied by a narrow pulse width upon impact. This suggests that in the absence of the mucus layer, the impact force is more concentrated and intense. As the adsorption time increases, there is a gradual decrease in peak acceleration and a broadening of the pulse width. This trend indicates that the mucus layer acts as a shock absorber, dispersing the impact force over a longer period, thereby reducing the peak force experienced by the sample. This finding has important implications for materials science and engineering, as it suggests that incorporating a similar viscous layer could enhance the impact resistance of materials.

Furthermore, the significant influence of adsorption time on energy dissipation is striking. Short-term adsorption of 1 and 5 minutes had minimal effects on energy dissipation, likely due to the insufficient formation of a stable mucus layer. However, as the adsorption time increases to 10 and 30 minutes, there is a substantial increase in energy dissipation rates. This suggests that a more extended adsorption period allows for a thicker and more uniform mucus layer to form, which in turn enhances its energy-absorbing capabilities.

This study aimed to investigate some interesting characteristics of the mucus in fish surface, with a focus on its potential research value in engineering applications, particularly in reducing surface drag for underwater vehicles. Mechanical and lubrication properties of the mucus film were tested using a nano scratch/indentation tester. Adhesion forces between the mucus and the fish scale were examined using AFM. In parallel, zeta potentiometer was employed to assess whether this adhesion force was derived from electrostatic interaction. Finally, a self-developed vibration excitation device was utilized to examine the vibration attenuation performance of the film, considering the significant underwater resistance caused by surface vibrations due to turbulence[20].

The fish's surface mucus, secreted by goblet cells on the skin, consists primarily of proteins, polysaccharides, and other trace substances[21, 22]. This mucus effectively adheres to the fish's scales, forming a protective mucus film. To assess changes in surface stiffness with indentation depth, indentation testing was performed using a nanoindentation instrument. Our findings, summarized in Figure 2 and Table 1, demonstrate that the mucus film exhibits a temporal adsorption pattern, with thickness increasing gradually with adsorption time. This mucus film enhances the fish's surface load-bearing capacity. As the mucus film thickens, it requires a higher pressure to puncture, indicating a stronger load-bearing capacity.

The adhesion experiment results (Figure 3) demonstrate a strong adhesion force between the mucus film and fish scales. And the Zeta potential electronegativity of the sample surface was rapidly reduced after the 1min short-term adsorption (Table 2), indicating a significant electrostatic effect during this process. In contrast, SF2, SF3, and SF4, which adsorbed for longer periods, had minimal impact on surface zeta potential electronegativity. Notably, there was no significant difference in surface potential values between SF3 and SF4. Combined with the results of adhesion properties testing, the adhesion force between films (MF-MF) was smaller than that of film-fish scale (MF-BF). This suggests that electrostatic interactions occur primarily during the initial 1min adsorption process. As the adsorption time increases, the continued adsorption of additional proteins in the initial layer leads to an increase in film thickness. However, this phenomenon is not driven by strong electrostatic forces, so its adsorption properties do not significantly enhance to the same extent as the film thickness. The adsorption behavior of these natural biological films seem to have a certain degree of similarity. Zhang et al. have conducted a study on the adsorption behavior of human natural mucus (saliva) on natural teeth, and their findings regarding the trend of changes in adhesion force are consistent with our results [16]. They proposed that adsorption among proteins primarily rely on weak hydrogen bonds and van der Waals forces, rather than the electrostatic interactions occurring between proteins and substrates. Additionally, Wang et al. studied the adsorption behavior of loach surface mucus on gold chip surfaces and found that the loach mucus first adsorbs on the substrate surface to form an initial film, followed by the proteins stacking to form a loose outer film that is easily washed away by buffer solution [23].

The results of the nano-scratch experiment indicate an excellent lubrication performance of the mucus film. After the adsorption treatment, the sample exhibits a significant improvement in reducing friction and wear. It should be noted that as the mucus film thickens, its anti-friction effect improves. However, this effect is inversely related to the adsorption time. The observation can be attributed to the fact that over time, proteins continue to accumulate on the sample surface, forming a looser outer layer that increases the frictional resistance when the needle tip moves laterally. Despite this, the wear reduction effect of the mucus film remains consistent over time, indicating that its lubrication ability is not diminishing. The exceptional lubrication performance of the mucus film is crucial for maintaining the high maneuverability of fish bodies. When swimming through river water or negotiating hard rock walls containing sand particles, it also serves to protect the fish body from potential scratching damage. Furthermore, there are significant differences in mechanical properties and film thickness between SF3 and SF4 samples treated with long-term adsorption and SF1 and SF2 samples treated with short-term adsorption, however, these differences do not show any additional contribution in lubrication. This suggests that the presence of long-term adsorption of mucus films may serve purposes beyond lubrication.

The vibration test results confirmed the hypothesis. As illustrated in Figures 6 and 7, when subjected to high g-value impact, the acceleration and energy dissipation of the SF1 were comparable to those of the control group. However, SF3 and SF4 samples treated with long-term adsorption significantly increased the acceleration pulse width, decreased the acceleration peak, and exhibited an increase in energy dissipation with increasing adsorption time. This suggests that SF1 and SF2 samples treated with short-term adsorption do not exhibit a vibration attenuation effect, whereas SF3 and SF4 samples treated with long-term adsorption show excellent vibration attenuation property. This is a crucial characteristic for the Asian carp, a kind of bottom-dwelling fish that has limited activity range and slow swimming most of the day, feeding on benthic small animals and plants. According to the lifestyle habits of the Asian carp, the mucus film on its body surface likely belongs to the "long-term adsorption group" in this study. When encountering danger or pursuing prey, the instantaneous acceleration of swimming can generate turbulence around the body, leading to surface vibration. At this point, the vibration attenuation property of the mucus film plays a important role, assisting Asian carp in overcoming the resistance caused by turbulence and enhancing swimming speed.

In the past few decades, the research on surface drag reduction of fish has primarily focused on exploring special structures on non-smooth surfaces to suppress turbulence. Illustrative study reveals that the surface of a shark's body comprises rhombically arranged shield scales interspersed with numerous minuscule grooves[5]. These grooves, by generating flow vortices, diminish surface momentum exchange and attenuate interfacial Reynolds shear stress. Simultaneously, there's an interaction between the groove structure and turbulence, leading to the generation of novel reverse vortex pairs, which further contribute to drag reduction[5]. Dolphin skin, on the other hand, is constituted of a sleek epidermal layer and a dermis rich in hollow mastoid structures[24, 25]. As turbulent frictional resistance escalates during swimming, the epidermal layer of dolphin skin undergoes micro-scale elastic deformations. This transformation progresses from a sleek surface to a papillary, non-smooth structure, forming a concave region that peaks, valleys, and peaks again. This concave formation spawns a clockwise rotating reverse vortex pair, consequently mitigating turbulent resistance. Our study also unveils that the surface mucus of fish plays a pivotal role in drag reduction and turbulent resistance suppression. These functionalities manifest in a gradient, extending from the exterior to the interior of the mucus film. As shown in Figure 8, during high-speed swimming, the outer layer, characterized by a thicker protein film, is responsible for vibration damping. Conversely, when encountering abrasive sand or stones, the sleek inner film serves to significantly curtail friction and wear. Theoretically speaking, the coupling effect between mucus and the specialized structures of non-smooth surfaces is a primary factor underlying the agile and efficient swimming observed in fish. And in our future research endeavors, we aim to delve deeper into the formation mechanisms, influencing factors, and potential applications.

The drag reduction and vibration attenuation performance of the fish’s surface mucus film has been studied using nano-indentation/scratch techniques and a self-developed vibration excitation device in this paper. Based on the given testing conditions, the conclusions can be summarized as follows:

(1) The adsorption of the fish’s mucus onto scale surface experiences two phases, short-term adsorption adsorption and long-term adsorption adsorption. The former is carried out through electrostatic interactiont, ultimately forming a smooth inner layer. As the adsorption time progresses , additional proteins gradually accumulate, forming a thicker outer layer (the latter).

(2) The inner layer of the mucus film exerts a significant lubrication property, effectively preventing the friction and wear caused by underwater sand and gravel. And the outer layer exhibits an exceptional vibration attenuation effect, aiding Asian carp in overcoming the turbulence-induced resistance, thereby enhancing their swimming speed.

Acknowledgments

This work was supported by the Science and Technology Research Program of Chongqing Municipal Education Commission (Grant Nos. KJQN202001309, KJQN202301345), the Natural Science Foundation of Chongqing (No. cstc2021jcyj-msxmX0812), the Opening Project of Engineering Research Center of Chongqing Education Commission of China in Running and Maintenance of Robots (No. YWZX20220002).

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No competing interests reported.

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Research on the drag reduction and vibration attenuation performances of the fish’s surface mucus film

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