Abstract
Develo** high-performance composite materials is of great significance as a strong support for high-end manufacturing. However, the design and optimization of composite materials lack a theoretical basis and guidance scheme. Compared with traditional composite materials, natural materials are composed of relatively limited components but exhibit better mechanical properties through ingenious and reasonable synthetic strategies. Based on this, learning from nature is considered to be an effective way to break through the bottleneck of composite design and preparation. In this review, the recent progress of natural composites with excellent properties is presented. Multiple factors, including structures, components and interfaces, are first summarized to reveal the strategies of natural materials to achieve outstanding mechanical properties. In addition, the manufacturing technologies and engineering applications of bioinspired composite materials are introduced. Finally, some scientific challenges and outlooks are also proposed to promote next-generation bioinspired composite materials.
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1 Introduction
Materials have evolved throughout human history, from the initial use of shells, bones and wood to today's replacement including a variety of metals, polymers and composites. The rapid development of society puts forward higher requirements for the performance of structural materials. However, certain properties of structural materials are mutually exclusive, such as the contradiction between strength and toughness [1]. In addition, it is worth considering how to achieve lightweight structural materials under the premise of ensuring strength. Fortunately, the long-term competition for survival in nature has driven the evolution of natural materials toward high strength, toughness, impact resistance and light weight, providing inspiration for scientists to solve these problems. For instance, bone and nacre achieve excellent strength and toughness simultaneously by utilizing multihierarchy structures and interface characteristics.
Almost all natural materials are composite materials, which are composed of a limited number of components with poor performance but can achieve significantly better properties than each component. In addition, natural materials are not simple mixtures of components. The basic reasons for the excellent performance of natural structural materials include the structure spanning multiple scales, the interface between different components and complex chemical compositions. The hierarchical structure spanning multiple length scales of nano, micro, meso, and macro has a synergistic enhancement effect. Similarly, multiple chemical components work synergistically instead of a single type of component to improve the performance of natural materials. Interfaces can arrest cracks, enhance flexibility and contribute to the viscous response of materials during deformation [2]. In addition, living organisms usually produce specific properties by combining multiple factors rather than a single factor. For instance, mollusk shells use aragonite and proteins to achieve a toughness improvement of several orders of magnitude beyond its component materials through the structure and interface characteristics of the brick-and-mortar [3]. Natural materials improve overall properties by positioning optimized components and structures in appropriate areas to adjust local properties. The properties in a single region are defined as local properties, such as strength, stiffness and hardness [4]. In addition, many diverse living organisms have evolved the same core features and design themes in response to natural challenges due to convergent evolution, such as the similar structures. Hence, it is beneficial to develop better structural composite materials by extracting the key features and combining them skillfully [5].
Bionics is a discipline that guides invention and creation by the study of biological structure, function and principle. Bionics provides a variety of strategies, such as modification of natural materials and biomimetic mineralization, for the preparation of new materials. Moreover, the development of biomimetic materials is closely related to the progress of advanced manufacturing technology, especially additive manufacturing, which effectively controls the manufacturing process at multiple scales [6]. In addition, electrospinning can more flexibly control the arrangement of nanofibers so that it has a great advantage in preparing nanofiber composites [7].
In this review, three basic factors that determine the excellent mechanical performance of natural materials, namely, structure, interface and chemical composition, are discussed, and how organisms achieve specific properties, such as impact resistance, fracture resistance, bending resistance and lightweight, are analyzed based on the above three basic factors. Then, the manufacturing strategy of new biomimetic materials and the application of bionic design in engineering materials are introduced in detail. Finally, the existing severe challenges and future development directions are presented.
2 Factors that Determine Natural Material Properties
Commonly, natural materials achieve specific properties by altering multiple factors, mainly including the composition, structure and interface [8] (Fig. 1). The different components and structures bring more flexibility to realize excellent performance to fit the environment [9]. In addition, materials with excellent mechanical properties and specific functions can be achieved by arranging and combining regions with diverse chemical compositions and structures in a regular order. The existence of an interface can act as a transition of two regions to avoid excessive interior stress. Hence, the multiple factors work together to improve the mechanical performance of natural materials [3, 10]. In this section, three important factors affecting the performance of natural materials are introduced in detail.
2.1 Chemical Compositions
Chemical composition is one of the most crucial factors for determining the performance of natural materials. Chemical characteristics mainly include mineralization, inorganic ions, biomole-cules and the degree of hydration. Adjusting the type and concentration of the components can have an important effect on the mechanical properties of natural materials. In addition, multiple compositions cooperate to enhance the performance of natural materials rather than a single type of component [16, 17].
There are significant differences in the degree of mineralization among various organisms to obtain specific traits to meet environmental challenges. Through different types and degrees of mineralization, local properties can be precisely and flexibly adjusted [17]. Natural materials with a high degree of mineralization include teeth and nacre. Radular teeth of chitons that exhibit increasing mineralization from the posterior to the anterior regions have achieved outstanding overall performance by altering mineralization to ensure smooth feeding without injury induced by abrasion [18, 19] (Fig. 2a). The combination of minerals in biological systems is an interesting subject of research but remains largely unexplored.
The regulation of composition to achieve different properties. a The gradient mineralization of radular teeth of chiton [18, 19]; b The distribution of different type of amino acid in the nereis jaws [22]; c The diverse site-specific modulus induced by distinction of hydration [24]; d The distribution of different ions in the fang of spiders [25]
In addition to biomineralization, the type, concentration and binding state of biopolymers can also control the mechanical properties of materials [20, 21]. The nereis jaw presents an inhomogeneous distribution of polymers, such as a remarkable variation in the amino acid content at different positions (Fig. 2b). These biomolecules interact with the corresponding ions to regulate mechanical properties. Hence, the mechanical properties of the nereis jaw show a notable gradient, with higher hardness from the base toward the tip [22, 23].
Hydration also plays a significant role in the process of regulating mechanical properties, which mainly depends on the hydration sensitivity of the protein. Water regulates the mechanical properties of natural materials by reducing interactions and interchain space. In addition, water can increase the fluidity of proteins by decomposing and replacing the hydrogen bound to the material inside, thus changing the deformation behavior of protein-based materials. In addition, water is able to constitute a network with protein to serve as plasticizers to reduce hardness [8, 21]. The beak of a squid is an attractive example of tuning mechanical properties with the transformation of hydration (Fig. 2c). The beak is composed of chitin, water and proteins without inorganic components. In addition, it is the hardest and stiffest known biomaterials, comprised of pure organic materials [24, 26]. A 200-fold increase in stiffness exists from the soft beak base to the maximum stiffness of the distal rostrum, which is tuned by the level of hydration [24, 27].
Ions can also participate in the enhancement of the mechanical performance of natural materials. Although the content of some ions is low in natural materials, their effect is crucial. In natural materials, the ions that take part in regulation are mainly metal ions, but other inorganic ions at times. Metal ions in natural materials mainly interact with biomolecules to form unique metal coordination bonds, a chemical interaction distinguished by common covalent and non-covalent bonding. This phenomenon is widely found between transition metal ions (e.g., Fe, Zn, Cu, and Ni) and proteins to generate metal coordination complexes. Hence, metal ions play a pivotal role in protein-based natural materials to provide enough protection, abrasion resistance and load-bearing performance. The unique mechanism of the interaction between metal ions and protein provides more possibilities for toughness, hardness and self-healing [16, 28, 29]. The type, concentration and distribution of ions can be adjusted flexibly to determine the mechanical properties [28]. For example, spider fangs obviously exhibit uneven distribution of ions (Fig. 2d). Energy dispersive X-ray spectroscopy map** reveals the distribution of Zn, Ca and Cl. Specifically, Zn and Cl show the same changing trend; that is, these elements are rich at the fang tip, while Ca is rich at the fang base. The difference in the properties of spider fangs notably corresponds to the distribution of ions [25].
2.2 Structure
In general, the mechanical properties of natural materials with similar compositions may differ because of their structure spans multiple scales. Natural materials mainly use changes in basic features, including arrangement, distribution, dimension, and orientation, to constitute different areas with various structures. In addition, the different structures in diverse regions customarily have different functions and properties, and then various regions combine along a certain sequence to form a unique architecture to satisfy requirements for survival.
Arrangement is a crucial element in creating diverse structures. For the same structural units, such as fibers, tubes, and plates, the diverse arrangements will directly cause differences in the structure of different locations [30, 31]. As shown in Fig. 3a, the reasonable arrangement of layers with different fiber directions significantly improves the toughness of the material by preventing crack propagation [5]. In addition, the shell of Chrysomallon squamiferum realizes remarkable mechanical properties by arranging multilayer structures with different mechanical performances and specific functions. In general, various structures with different arrangements have distinct characteristics, such as Bouligand structures that provide toughness and in-plane isotropy and suture structures that control flexibility and strength.
The different methods regulate the structure of biological materials to achieve different properties. a The material toughness is improved by reasonable arrangement of layers with different properties [5]; b The squid sucker ring teeth alter the distribution of pores to control the properties precisely [32]; cThe teeth of parrotfish exhibit diverse properties in different region through altering the orientation and dimension of mineralized fibers [38]; d The molar tooth of crayfish with the diverse orientation in distinct areas exhibits different mechanical properties [45]
Some natural materials evolve their multiple structure units with helical, layered and tubular structures. The distribution of these structural units is closely related to the performance of natural materials. For instance, the distribution of tubes and pores directly determines the density of natural materials. The rational distribution of tubes and pores will extremely reduce the mass of natural materials without loss of mechanical properties. In addition, the distribution of reinforcements, such as fibers, rods and sheets, has an important influence on the local mechanical properties, which appear at weak locations or high stress areas to make natural materials more durable and robust [10]. Squid sucker ring teeth, which are used as a tool to capture and handle prey, are representative materials that can realize the balance between performance and light weight by altering the distribution of pores (Fig. 3b). The porosity increases notably from the exterior to interior, followed by a decrease in the relative modulus and hardness [32, 33]. The core with more pores combines with a dense periphery, which can clearly enhance bending stiffness. Besides, many biological materials alter the distribution of tubes used as energy-absorbing devices to fit the function of natural materials, such as sheep horns [34, 35], hoof walls [36] and tooth dentin [37].
The dimensions of constituents directly determine the performance and functions of natural materials. Commonly, the variation in lamellar thickness and fiber diameter is mainly responsible for the complex and multiple structures of natural materials. For instance, parrotfish feed by biting stony corals, whose tooth present distinct gradient mechanical properties obviously (Fig. 3c). A schematic representation of the polarization-dependent imaging contrast map** indicates that the average diameter of fibers presents an clear decrease toward the tip of the tooth (from 5 to 2 \(\mathrm{\mu m}\)). Corresponding to this trend, the hardness and stiffness increase from the tooth base to the tip, which improves the wear resistance of the tooth surface. The region that invariably contacts stony corals suffers larger abrasion. This feature of parrotfish makes their teeth more durable under use conditions [38]. In a similar example, a sponge spicule consists of a central core of hydrated silica that is surrounded by concentric layers of silica and a protein material whose thickness decreases from the core to the edge of the sponge spicule [39].
Orientation is another major factor that can form microstructure with different local properties [40]. The orientation of units, such as fibers, platelets, and tubules, commonly exhibits obvious anisotropy, and is closely related to the local properties of natural materials. The preferred orientation of units is the result of natural selection induced by the magnitude and direction of loading. In addition, natural materials are good at utilizing the transformation of the orientation to build a unique architecture with certain roles to enhance the overall performance. The most typical structure is the Bouligand structure which is formed by twisting fibers layer by layer to dissipate energy efficiently and avoid the catastrophic propagation of cracks [41, 42], such as crab [43] and lobster [44]. In another example, the molar tooth of crayfish also utilizes the orientation of fibers to realize outstanding mechanical performance (Fig. 3d). The chitin fibers near the surface run perpendicular to the surface, which is coincident with the direction of the load. By adjusting its surface properties, the preferentially oriented and highly mineralized region with a higher modulus and hardness provides enough support for tearing prey. In contrast, the fibers in the deeper layers are parallel to the surface with low mineralization to dissipate energy to protect the tooth from catastrophic fracture [45].
2.3 Interface Characteristics
Interfaces commonly act as junctions between two regions with diverse compositions and structures to obtain more toughness and durability in natural materials. The natural materials form a continuous transition between different components through ingenious interface design and achieve a smooth transition of properties between diverse components. The interface can effectively reduce the stress concentration and shift the direction of crack extension to improve the toughness of natural materials [46].
Mechanical characteristics at interfaces play an important role in determining interfacial properties. The properties of interfaces can be tuned by adjusting the interfacial mechanical characteristics, including interlocking and altering roughness. Mechanical characteristics commonly depend on the behaviors of the interlayer, such as sliding, shearing and friction, to realize the purposes of energy dissipation. Moreover, crack propagation can be further controlled by only altering the interface (Fig. 4a). Nacre is a typical example of a natural material with excellent strength and toughness owing to its unique “brick-and-mortar” microstructure; this material is commonly imitated to develop artificial composites with outstanding performance [47]. The abundant mineral bridges are embedded in the organic matrix to concatenate the adjacent lamella, increasing energy dissipation during the progress of “pull-out” of mineral bricks. In addition, the interlocking of tablets leads to more deformation during sliding, which endows nacre with the ability to dissipate more energy to increase its toughness. In addition, the nanoasperities on the surface of platelets facilitate energy dissipation through interlayer friction between two rough platelets. Through synergies of several principles, nacre can flexibly tunes its interfacial properties to tolerate damage efficiently [48, 49].
The interface with ingenious connection to adjust material properties. a The multiple mechanical behaviors of nacre are used to enhance the interfacial properties, including breaking of mineral bridge, inelastic shearing of nano-asperities, deformation of biopolymer and tablet interlocking during sliding to dissipate energy efficiently [3]; b The chemical characteristic in the interface to promote mechanical performances through cross-linking between metal ions and biomolecules, such as protein, chitin and cellulose [50]; c The diverse tiny structures in the different interface in the oyster reefs connected with two shells robustly. One is gradual interface, and the other is sharp interface [51]; d The byssus cuticle of marine mussels utilizes cross-linking forming Dopa-Fe bond and subtle structures of phase separated domain to obtain the remarkable interfacial properties [52]
Chemical characteristics of the interface primarily play a role through the way of cross-linking and hydrogen bond. As shown in Fig. 4b, small amounts of ions and minerals (e.g., Zn, Mn, Cu, Ti, Al, and Fe) participate in the assembly of materials and reinforce the delicate structure by the strategy of synergic cross-linking/coordinating. These metal ions cooperate with protein and biopolymer chains, such as chitin and cellulose, to form stochastic helices and coils, generating metal-protein/polysaccharide compounds with high stability, which play a key role in strengthening. Hence, natural materials utilize this strategy to manage their local properties wisely. This cross-linking is obviously detected in the materials consisting of silk and cellulose and other organic matrices. In addition, hydrogen bonding is also commonly used to strengthen materials in nature [28, 50]. In summary, chemical characteristics tune the properties of natural materials at the molecular level to achieve strengthening and toughening.
The structure is also a marked characteristic to make a distinction between diverse interfaces. The oyster reef is an excellent example of utilizing unlike interfaces to connect two shells (Fig. 4c). An effective adhesive is used to build reef communities with outstanding performance to confront storms and surges. Backscatter electron imaging is used to show the diverse structures at two shell-adhesive interfaces. However, beyond that, the dimensions of the prisms at the interfaces also exhibit marked differences. The local structures at the interface bring better overall performance to the function of materials [51]. Thus, living organisms build artful junctions between diverse materials by altering the structure at the interface to achieve optimal overall properties.
The interface of natural materials commonly utilizes multiple factors to realize the enhancement of interfacial properties. The diverse factors work together to obtain multifaceted advantages for natural materials meeting the requirements of certain functions. The byssus cuticles of marine mussels are representative examples of biological materials that display excellent mechanical properties due to the unique interface with the ingenious structure and cross-links (Fig. 4d). There are many granular areas in the protein matrix of the byssus cuticle. Under the action of a load, the regions of the micro phase-separated construction deform greatly and dissipate a large amount of energy. In addition, the cross-linking between dihydroxyphenylalanine (DOPA) and Fe ions significantly enhances the properties such as hardness and stiffness in regions [52, 53].
3 Strategies of Natural Materials to Achieve Excellent Mechanical Properties
Different natural materials have evolved various mechanical properties due to the tremendous difference in living environments. The multiple functions of natural materials make living organisms more confident in getting food, resisting enemies and surviving in some special conditions [54]. For instance, the light weight of most birds for flight [13], abrasion-resistant teeth [55] and the protective effect of natural armors [56] are typical examples of natural materials with specific functions for survival. The various functions are realized by ingeniously regulating structures, interface characteristics and chemical composi-tions to confront distinct challenges. In addition, the diverse functions commonly depend on different local properties, so distinct local properties and diverse combinations of site-specific properties make natural materials more flexible and robust to realize specific functions for various working conditions. For instance, the natural material that sustains frequent wearing commonly possesses a higher surface hardness. The natural material suffering from an extremely high local load has a specialized layer to homogenize the stress to prevent stress concentration. Artificial materials can draw lessons from natural materials with specific functions by combining and arranging different regions with diverse local properties for engineering applications in distinct working situations. In this chapter, the strategies of biological materials to achieve specific functions and their potential applications in engineering are introduced.
3.1 Multilevel Energy Dissipation for Impact Resistance
In nature, natural materials inevitably withstand enormous impact forces, such as the smasher of mantis shrimp hammering prey [57,58,59], the pecking of trees by woodpeckers [60] and the elytra of beetle [61]. The impact loads lead to a substantial impact force directly acting on the surface of natural materials and readily induce a high level of stress concentration. Because the force acting on the impact surface is very large, a high hardness and strength of the impact surface are necessary to resist the direct destruction of the impact. However, a homogeneous component with high hardness and strength is inadequate because of the lack of toughness resulting in fracture. Hence, the region with enough toughness to dissipate impact energy effectively is also indispensable for avoiding catastrophic fracture and increase durability. In addition, the unique areas of some natural materials possessing particular local properties are mainly responsible for redistributing stress and strain to avoid stress concentration and excessive local strain. The smart transition of local properties spanning various areas results in diverse regions with different effects during the impact process and cooperatively resists impact damage. Furthermore, some microscopic characteristics of the inherent properties of components themselves also significantly affect the response behavior to impact loading, such as the crystallographic characteristics of biominerals and the properties of biopolymer chains [62,63,64]. Similarly, the outstanding impact resistance is also the result of precisely regulating the local properties and functions controlled by multiple factor synergies, such as structure, composition and interface. Multilevel energy dissipation can effectively reduce the impact energy of a single region, thereby improving impact resistance.
The dactyl club of mantis shrimp can destroy the rigid biological armor of mollusks under the impact of a high strain rate, which achieves accelerations over 10,000 g and reaches speeds of 23 ms−1 from the rest position [58]. In addition to the contribution of the herringbone and Bouligand structure that has been reported, another important reason for the high impact resistance of the dactyl club of mantis shrimp was recently found to be the impact-resistant nanoparticle coating on its surface [65] (Fig. 5a). The nanoparticle coating is composed of tightly packed ~ 65 nm bicontinuous nanoparticles of hydroxyapatite integrated within an organic matrix. High strain rate impact results in the rupture of nanoparticles into smaller primary grains (~ 10–20 nm), which dissipates part of the impact energy. Differential interference contrast optical micrographs reflect rough surfaces of the clubs after impact, indicating that particle translation and ablation are also the underlying mechanism of energy dissipation [65]. Some microscopic characteristics of the inherent properties of components themselves directly determine the impact resistance of natural materials, especially crystallographic features of biominerals. For instance, during the impact process, deformation twinning and partial dislocations are found in nacre to combat catastrophic fracture under impact loading with a high strain rate [64, 66].
Natural materials achieve remarkable impact resistance through multilevel energy dissipation. a Another important factor for impact energy dissipation of the dactyl club of mantis shrimp is the impact resistant nanoparticle coating on its surface [65]; b The layered structure of the beetle cuticle resists impact [69]; c The unique structure of coconut protect the internal fruit form the injuring of falling from the tree, mainly including vascular bundles and concentric rings of hollow fibers to dissipate impact energy effectively [72, 73]
Except for the mantis shrimp mentioned above, another classic example of significant impact resistance is the insect cuticle. The insect cuticle has a multilevel laminated structure with different stiffness gradients, which can be used as a defensive armor to resist the impact of predators. Previous studies have shown that the structure of the insect cuticle is usually composed of the epicuticle, exocuticle and endocuticle [67]. In contrast, the epicuticle is stronger and can effectively avoid impact damage to the stratum corneum, while the endocuticle is more flexible, which is conducive to dissipating impact energy and preventing crack propagation. However, the latest research shows that Pachyrhynchus sarcitis kotoensis has an inner layer that is stiffer than the outer layer. Researchers have provided the first evidence that a harder endocuticle can increase the mechanical properties of the cuticle, which gives us a deeper understanding of insect cuticles and provides new solutions for the design of biomimetic materials [68]. Besides, **ng et al. revealed the impact resistance strategy by studying the mechanical properties of the layered structure of a beetle cuticle under impact load. The discontinuity at the cuticle interface and the distribution of the stiffness gradient are beneficial for preventing stress wave propagation and improving impact resistance [69] (Fig. 5b). The above research shows that the impact energy can be effectively dissipated among the layers through a reasonable distribution of stiffness between the hierarchical structures, which provides an important inspiration for designing structural materials with higher impact resistance. For example, inspired by the stiffness gradient of insect cuticles, researchers have designed an impact-resistant structure with programmable stiffness [70]. In addition, Rivera et al. investigated the mechanism of how the elytra of Phloeodes diabolicus greatly improves impact resistance. In addition to the stiffness gradient on the macroscopic scale, the mechanism highlights the influence of the interface microstructure. Specifically, the ellipsoidal geometry and laminated microstructure provide mechanical interlocking at the interface, thus avoiding catastrophic damage [71]. Therefore, this research provides bionic inspiration for our design of connections in engineering applications. At present, research on beetle elytra has made many achievements, but the structural characteristics of smaller-scale elytra remain to be explored.
Additionally, another typical natural material with excellent impact resistance is coconut, whose fruits are protected by the wall with three layers from impact upon falling from trees, including the exocarp-like leather, fibrous mesocarp and hard endocarp (Fig. 5c). The first two layers mainly provide a function of dissipating energy and buffering the tremendous impact. The ripe endocarp, with a unique structure, directly in contact with the coconut is hard and tough enough to guard the fruit from injury. The structure of the endocarp ingeniously transfers loads to cellulose crystalline nanostructures rather than vulnerable fruits. In addition, the rupture of the vascular bundles provides generous energy dissipation to prevent catastrophic fracture and enhance toughness [72, 73]. The advantage of the coconut shell structure is that it consists of three layers with different structures and functions; this provides a good example to study the control of the impact resistance of multiscale hierarchical shell structure.
Impact damage is very common in the automobile, construction, national defense and sports industries, so how to realize the effective and rapid dissipation of impact energy inspired by biology has great significance for modern engineering. The deep study of natural materials can provide inspiration for the development of new impact-resistant materials.
3.2 Biological Toughness for Fracture Resistance
Fracture is one of the most dangerous modes of failure and can directly result in materials invalid. Hence, it is vital to prevent the emergence and propagation of cracks by altering the structure, composition and interface. The ability to resist fracture is commonly related to the toughness of natural materials. A higher toughness means more energy consumption during the process of failure, which indicates that it is more difficult to drive the propagation of cracks. Natural materials usually adopt intrinsic toughening and extrinsic toughening mechanisms to effectively improve the fracture resistance [74].
According to traditional fracture toughness theory, fracture toughness refers to the ability of a material to prevent crack extension [75]. Generally, crack extension occurs when the crack driving load equals or surpasses the crack propagation resistance of the material. Notably, the crack growth resistance and crack driving force are both dynamic, especially for natural materials with various components and microstructures, which makes the fracture process a complicated and changeable process [75]. The regulation of the local modulus is conducive to fracture resistance [76]. In addition, specific interfaces, such as weak interfaces and sacrificial bonds, also significantly increase the fracture resistance of natural materials. Furthermore, different from the foregoing internal toughening mechanism, external toughening, such as fiber bridging, primarily prevents crack propagation by increasing crack extension resistance [76].
Natural materials generally achieve excellent fracture toughness by combining intrinsic and extrinsic toughening across multiple scales. For instance, the baleen of whales can substitute teeth and serves as a filter for food with outstanding fracture resistance without replacement throughout life [77] (Fig. 6a). The unique sandwich-tubular structure, hydration and gradient mineralization are crucial reasons for its remarkable fracture toughness. In addition, by increasing the interchain space and decomposing secondary bonding, the interaction between water and matrix protein significantly improves toughness. Hence, the combination of various factors contributes to the notable fracture resistance of the whale baleen. In addition to the baleen of whales, the compact bone of the elk antler is another typical example utilizing intrinsic and extrinsic toughening to promote the fracture toughness of natural materials [11, 78] (Fig. 6b). In antler bone, intrinsic toughening is generated by the stretching and unwinding of mineralized collagen at the nanoscale and continuous sliding between collagen molecules and hydroxyapatite particles at the microscale. Extrinsic toughening to resist fracture mainly depends on the deflection and bridging of cracks commonly operating at the micrometer scale and even above [78].
The materials mentioned above are initially in a condition without cracking, so the process of failure mainly inhabits the nucleation of cracks in the first step. Instead, some natural materials make use of cracks to realize specific functions ingeniously, such as spiders [31, 79] (Fig. 7a) and scorpions [80, 81] (Fig. 7b). The spiders and scorpions commonly possess a crack-shaped slit near their leg junction to catch extremely weak vibrations. The existence of inherent cracks puts forward the higher requirement of the ability to prevent the propagation of cracks. As shown in Fig. 7b, the slits of scorpions adopt a mechanism to prevent the propagation of cracks spanning multiple scales. The subtle layered structure resembling those of other natural materials near the slits notably promotes fracture toughness. In addition to the layered structure, the unique cuticular membrane covering the slit plays a significant role in avoiding catastrophic structural failure. Compared with the lower modulus, the rational modulus of the membrane makes the elastic modulus of the whole biocomposite steady during the deformation process of, and the opening of slits remains in a certain range throughout the deformation of the membrane. The unique structure with site-specific properties endows the slit sensors of scorpions with an excellent ability to effectively combat fractures [80, 81].
Living organisms utilize crack-shaped slit to sense tiny vibration and ensuring safety of materials simultaneously. a The crack-shaped slit in spider legs to sense vibration in case of ensuring safety of crack-shaped slit [31, 79]; b The basitarsal compound slit sensilla of scorpions prevent the propagation of crack-shaped slits through the unique structures and the membrane ensuring the safety of their sense organs [80]
As a quite common and threatening failure mode in the engineering field, fracture seriously affects people's lives and production, causes great economic losses, and even threatens personal safety. Therefore, it is extremely important to improve the fracture toughness of engineering materials inspired by natural materials.
3.3 Biological Gradient Increases the Area Inertia Moment for Bending Resistance
Many natural materials are susceptible to failure due to bending and buckling, such as beams and poles with a high aspect ratio. Although recoverable bending does not result in irreversible failure, large bending also means that natural materials cannot be used properly for a period of time. In addition, excessive buckling will directly lead to the instability of materials. Therefore, bending and buckling must be controlled effectively for normal use and to avoid failure. Natural materials can normally obtain remarkable flexural strength through biological gradient structures [82]. The deflection y can be calculated by Eq. 1:
where E is the elastic modulus, M is the bending moment, and I is the area moment of inertia. In addition, Euler’s buckling equation is typically used to evaluate the level of buckling. The overall buckling under loading is generally satisfied by Eq. 2:
where \({P}_{cr}\) is the critical load, L represents the length of the biological materials and K is a constant dependent on the column-end conditions. Hence, the bending and bulking resistance is tightly related to the local modulus and area moment of inertia. The elastic modulus is commonly tuned by altering the components of materials, while the area moment of inertia is determined by the distribution of mass. In other words, the local density directly determines the area inertia moment and further inflects bending and bulking resistance. In terms of the above expression, a larger area moment of inertia means a greater capacity to withstand bending but worse bucking resistance. Therefore, there is a contradiction between bending and buckling. In nature, many materials utilize gradient methods to distribute their mass ingeniously, obtaining remarkable stiffness with a light weight to resist deflection with a hollow core and foam. On the other hand, the problem of bulking resistance is solved by adding the reinforcement, such as disks, struts and stiffeners, at a proper location to resist excessive local bucking [83].
Flight feathers, composed of a cortex of a solid keratinous shell, enclosing the medulla of a foamy core, are mostly subjected to bending during flight. The cross section of a seagull feather from calamus to rachis shows that the shape of the cortex changes from circular to rectangular (Fig. 8A). Compared with the circular hollow beam, the hollow beam with rectangular cross sections has advantages of higher bending stiffness per unit area and a stronger resistance to changing cross-sectional shape. The cortex of the rachis is similar to an I-beam that distributes material to the area of the maximum area inertia moment to resist bending deformation [84]. Similarly, feather shafts of other volant birds, such as pigeon and bar owl, also exhibit such a shape factor gradient [85]. This variable cross-sectional structure of feather shafts not only resists bending deformation but also has the advantage of light weight.
The gradient strategies of natural materials for achieving outstanding bending resistance. a The cross section of seagull feather gradually changed from round to rectangular to resist bending [84]; b The stem of palm exhibits the increase in relative density from center to surface, resulting in the different strength to resist bending [4, 8]; c The bamboo tunes the distribution of fibers resulting in the gradient flexural modulus to confront bending with a low mass [88, 89]
The stem of a palm is a typical example of using the gradient method to gain bending stiffness (Fig. 8b). Palms acquire excellent overall resistance to bending and buckling by controlling their local density. The relationship between mechanical strength \({\sigma }_{c}\) and \(r\) can be described as \({\sigma }_{c}\propto {r}^{4}\), where \(r\) represents the radius of the palm and stress \(\sigma\) complies with the \(\sigma \propto {r}^{6}\) relationship. Besides, palms show the trend that the exterior density is higher than that in the interior by utilizing the uneven porosity. Compared with homogeneous materials of equal quality, the overall bending stiffness is increased by 2.5 times [4].
Figure 8c demonstrates that the distribution of fibers across the thickness of bamboo is nonuniform, resulting in the outer portion of the bamboo being more dense than the inner portion. This hierarchical architecture induces functionally local properties along the direction of thickness. For instance, the stiffness increases toward the surface, resulting in more flexible rigidity of the stem [86,87,88,89].
Bending and buckling are common in machinery, such as the drive shafts of cars and machine tools, which seriously reduce the transmission accuracy and even cause mechanical failures, threatening personal safety. Therefore, it is significant to learn strategies for resisting bending and bulking of natural materials to improve mechanical properties.
3.4 Biological Hollow Structure for Lightweight Materials
Natural materials generally have excellent mechanical properties and are lightweight to satisfy the needs of survival. For example, the demand for flight requires a bird with lightweight wings and bone to satisfy relevant aerodynamic requirements [90]. Living organisms utilize all kinds of methods to decrease quality under the prerequisite of ensuring related mechanical performance. Hollow structures, such as pores and holes, can significantly reduce the quality of the material. However, if the distribution of hollow structures is unreasonable, then the mechanical properties of materials will be inadequate. Therefore, some ingenious strategies should be employed to adjust the properties of materials [91].
Many birds have hollow bones for the purpose of decreasing the mass to ensure flexibility of flight [92]. The wing bone of a bird is a typical case that adjusts the local structure of materials to realize lightweight whole materials on the macroscopic scale [13]. The cross sections of wing bones of Turkey vultures show that the cross-sectional shape of the wing bone changes significantly with position (Fig. 9a). The cross-sectional shape is observed as a hollow circular section, which varies toward the end of bones. The various cross-sectional shapes of bone ensure the mechanical performance of different locations to withstand unequal forces. The wing bone of birds obtains excellent performance in responding to severe environmental challenges through precise control of the cross-sectional shape.
The hollow structure strategies of biological materials realize lightweight with excellent mechanical properties. a The wing bones of Turkey vulture realize the unity of lightweight and strength by adjusting the shape of hollow area [13]; b The wood with the smart cellular structure combine outstanding mechanical properties and lightweight simultaneously [141]; d The novel dactyl-inspired helical-fiber sinusoidal-structure laminate was manufactured based on the Bouligand and herringbone structure [143]
In addition, there is a high demand for glass in production and life, but it has the shortcomings of low toughness and poor impact resistance. Tempering and laminating, as a conventional way to improve the impact resistance of glass, cannot effectively solve the problem of glass fragility. Yin et al. designed a laminated glass inspired by the brick-and-mortar structure of the nacre of the mollusk shell [137]. The impact resistance of the glass was significantly improved by utilizing the relative sliding between microscopic mineral tablets bonded together by biopolymers; at the same time, the high rigidity, bending strength and transparency were retained. Furthermore, the microstructures of fish scales and the cuticle of arthropods can also be used as laminated structures of glass to prepare strong, tough and transparent glass. Researchers have utilized laser engraving to fabricate glass with four bionic structures: crossply, Bouligand, segmented Bouligand and nacre-like. The impact tests of bionic glass show that the mechanical properties of glass can be significantly improved by regulating the dimensions of glass building blocks and adopting a mixed design combining plain layers and building layers [138] (Fig. 13b).
The design and manufacture of lightweight and tough body armor have attracted widespread attention with the rapid development of military technology. To date, fish scales, nacre, conches, crustaceans, exoskeletons and cortical bone have been investigated for the application of bulletproof components [140]. In addition, pangolin scales are arranged in an overlap** hexagonal shape around the central scale, which has important guiding significance for the design of protective armor. Moreover, at the nanoscale, the adjacent lamellae of the scales form an interlocking interface due to the suture-like cell membrane complex between keratinized cells [141] (Fig. 13c). A higher requirement for biomimetic engineering materials is needed to meet the integration of multiple functions in the field of military protection.
In other respects, a new type of crash box mimicking human tibia was prepared, which is composed of a concave structural shell and an inner core filled with negative Poisson's ratio structural material [142]. Inspired by the sinusoidal structure of the impact region and the spiral structure of the periodic region of the dactyl club of mantis shrimp, Han et al. made a novel helical-fiber sinusoidal structure laminate by coupling the two structures together that can be used for aircraft wings and car shells to improve their impact resistance [143] (Fig. 13d).
In general, bionic design provides a steady stream of inspiration for the design and manufacture of engineering materials. However, it is a severe challenge for designing and manufacturing engineering materials to achieve the unity of excellent mechanical properties and particular functions by imitating natural materials.
5 Conclusion and Perspective
Natural materials achieve outstanding mechanical properties by adjusting the three basic factors of structure, composition and interface to satisfy diverse requirements for survival [10]. Although natural materials are made from a limited number of materials, they tend to exhibit excellent mechanical properties many times better than the individual components due to the components of rational distribution, structures of ingenious arrangement and interfaces of precise junctions. Nature has provided us with many successful examples of organisms with specific functions, which adjust the properties of the material through the three basic factors to further achieve the desired specific function. Hence, the strategy of achieving high performance of natural materials can inspire us to design and manufacture structural materials with remarkable mechanical performance, such as high strength, high impact resistance and lightweight. However, the design and preparation of biomimetic materials still face numerous challenges.
First, it is extremely important to conduct more in-depth research on the mechanism of natural materials with excellent properties. The chemical compositions, structures, interface characteristics, and resulting mechanical and functional properties under living conditions still remain to be explored for a wide range of natural materials.
Second, although recent advances in materials and manufacturing have led to new synthetic materials exceeding the performance of their natural counterparts, most manufactured biomimetic materials lag far behind the performance of their natural materials [144]. Further advances in nanoscale material manufacturing and other advanced manufacturing technologies may provide new opportunities for the development of biomimetic materials, but new technologies also face the problem of large-scale production.
Third, living organisms can actively respond to external stimuli. Therefore, we should not only imitate their excellent mechanical properties but also imitate their self-healing and self-adaptation properties, which puts forward higher requirements for the design of the next generation of intelligent composite materials with multiple functions [145].
In short, the development of bionic composite materials is full of opportunities and challenges. On the one hand, with the continuous development of advanced manufacturing technology and equipment, the mechanism of the excellent performance of natural materials will be more deeply revealed. On the other hand, the existing preparation methods still face a series of problems, such as immature processing technologies and difficulties in large-area preparation. In the future, the intelligence of biomimetic composites should also be considered to make real use of biological intelligence, and there is still a long way to go before practical engineering application.
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Acknowledgements
Peng X X and Zhang B J contributed equally to this work. This work was supported by the National Key Research and Development Program of China (No. 2018YFA0703300), the Foundation for Innovative Research Groups of the National Natural Science Foundation of China (No. 52021003), Jilin University Science and Technology Innovative Research Team (No. 2020TD-03), the Natural Science Foundation of Jilin Province (No.20200201232JC), Interdisciplinary Integration and Innovation Project of JLU (No. JLUXKJC2021ZZ03) and “Fundamental Research Funds for the Central Universities”.
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Peng, X., Zhang, B., Wang, Z. et al. Bioinspired Strategies for Excellent Mechanical Properties of Composites. J Bionic Eng 19, 1203–1228 (2022). https://doi.org/10.1007/s42235-022-00199-9
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DOI: https://doi.org/10.1007/s42235-022-00199-9