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5 CONCLUSIONS AND RECOMM~NI)ATIONS: SCIENTIlilC AND TECHNOLOGICAL OPPORTUNITIES Biological structures are characterized by hierarchical architectural designs in which organization is controlled on length scales that range from the molecular to the macroscopic. These materials are multifunctional and are produced in situ at room temperature and atmospheric pressure. Many such structures are self- healing and remarkably durable, and many display properties that change in response to a changing environment; features of biological materials that represent desirable, and as yet unattainable, objectives in the design and manufacture of synthetic materials systems. Nature is parsimonious in its use of constituent materials, it returns to these same materials again and again to realize an astonishing range of structure and function. The utility of many synthetic hierarchical materials is limited at the present time by shortcomings in fabrication technology and resultant finished-part costs that are high. This is especially true for very high performance materials, that is, continuous fiber-reinforced composites (polymer, ceramic, metal matrix, etc.), materials designated for use under environmental extremes, and parts that need to function reliably for extended time periods. Similarly, there is always a need for more-efficient and more-sophisticated system designs, for applications ranging from improved performance aircraft and spacecraft to faster switching communication devices. 93

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94 Hierarchical Structures in Biology as a Guide for New Aiatenals Technology The Committee on Synthetic Hierarchical Structures concludes that the study of biological materials will provide many lessons for use in the development of new materials technologies. In some instances, this may take the form of direct utilization of biological materials or biosynthetic pathways; in other circumstances, biology will provide inspiration for the creation of new designs and new methods of fabrication. Some preliminary successes of this kind are described in chapters 3 and 4 of this report. The analysis of lessons learned from natural material systems could lead to the development of new classes of synthetic materials, improved processing technology, and innovative design and analysis approaches. MATERIALS The hierarchical architectures of biological materials systems rely on critical interfaces that link structural elements of disparate scale. The study of such systems reveals extraordinary combinations of performance properties, as well as limitations due to the modest thermal and chemical stabilities of biological molecules. A pplication of hierarchical design concepts to more-robust synthetic building blocks provides promising routes to high-performance adhesives and composites, biomedical materials, highly specific membrane and filtration systems, low-friction bearings, and wear-resistant joints. Specific opportunities and needs for materials development that were identified in previous chapters include: . . synthetic constituents to produce hierarchical materials with useful performance over a broad range of environmental conditions; low-friction and wear-resistant materials for joints and bearings;

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Conclusfons and Recommendations . 95 adhesives that mimic the tenacity and toughness of biological adhesives; and composites with high volume fractions of reinforcements. PROCESSING Biological structures are fabricated via highly coupled, often concurrent, synthesis and assembly In the conception and, evaluation of synthetic and processing schemes for new materials systems, the prospects for integrated system fabrication should be carefully considered. Specific needs to realize the full promise of integrated fabrication methods include: concurrent materials synthesis and structural assembly; processes to fabricate highly specific synthetic membranes and filters; use of cells to synthesize and deposit materials; biosynthetic pathways to the cost-effective manufacturing of new classes of shaped hybrid composites; and biosynthetic concepts and materials for self-repair of critical components and devices. DESIGN AND ANALYSIS Biological structures perform as parts of integrated systems and undergo continuous evaluation and refinement based on system performance In analogous fashion, considerations of integrated systems design and performance will take on increasing importance in the

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96 Hierarchical Structures in Biology as a Guide for New Materials Technology high-technology materials-related industries of the future. Interdisciplinary teams of scientists and engineers will be required to effectively design and develop structural systems with such complex architectures. The committee recommends that the academic and industrial sectors of the materials community prepare for this development through implementation of appropriate educational and engineering programs that are based on systems concepts. Several universities have recognized the promise of this approach and have developed programs to address these needs. Although, due to the diversity of the field, bioengineering curricula may vary in detail, they all strive to bring together the biologists' knowledge of physiology, anatomy, biochemistry, and molecular biology with the engineers' knowledge of design and structure (Watanabe, 1993~. Lessons to be learned from the design of natural systems include: strong, durable interfaces between hard and soft structural components; tribological joints with low friction coefficients and remarkable durability; mechanistic understanding and analysis methods for deformation and failure of complex systems; energy-absorbing mechanisms of rigid biological composites; platelet and surrounded plate analytical concepts; and moisture-friendly synthetic systems. SCIENTIFIC OPPORTUNITIES The hierarchical structures observed in biological systems represent potential solutions to the problems of materials choice,

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Conclusions and Recommcnda~'ons 97 materials fabrication, and component or system design that are currently limiting the utility and implementation of many modern materials and design concepts. Although the prospects for new biologically inspired materials technologies are real, full exploitation of this approach will require advances in engineering, education, and enabling science. Although there is a broad range of technologies that may contribute to the understanding of biomaterials, the committee recommends concentration on developments in structural biology, interface science, synthetic methodology, instrumentation, modeling, and theory to enhance the development and applications of hierarchical systems that are based on natural analogies. Some instances in which the translation of hierarchical structures found naturally might significantly impact materials science and technology are described below. Synthetic Methodology As discussed in Chapter 3, the design and preparation of hierarchical materials will place a new premium on the synthesis of macromolecules of precisely defined primary structure and complex chemical composition. At present, the only methodology available for the preparation of such polymers involves the use of gene synthesis and recombinant-DNA technology to create artificial structural proteins. This methodology is powerful and may lead not only to the creation of polymeric materials with functions not obtainable through conventional synthetic methods but also to an understanding of how control of molecular structure and function can improve materials performance. However, it is clear that the thermal and hydrolytic sensitivities of proteinaceous materials will limit their applicability in many important synthetic materials applications. Generalization of the methods of controlled synthesis to new classes of monomers thus becomes an important objective. Some initial developments along these lines may be foreseen. It has been known for many years that certain analogues of the natural amino acids can be incorporated into bacterial proteins with high

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98 Hierarchical Structures in Biology as a Guide for New Materials Technology fidelity (Cowie and Cohen, 1957), and it is likely that additional examples will continue to be identified. As further information becomes available regarding the mechanisms of transfer RNA charging and proofreading, the rational design of amino acid analogues useful in protein biosynthesis can be anticipated. Some first steps toward templated polymerization of other monomers have also been reported. Schultz and coworkers (Noren et al., 1989) have recently described a method whereby suppressor transfer RNAs that are chemically acylated serve to deliver unnatural amino acids to messenger RNA templates in an in vitro translation system. In this initial report, the method succeeded for X-amino acid analogues but failed when applied to ,B-amino acids. Despite this limited success, such methods offer a basis for systematic studies of templated polymerization processes. Progress in this area must be accompanied by advances in cell-free translation methodology if any impact on materials synthesis is to be made, since current cell-free methods are limited to the preparation of submilligram quantities of material. Looking beyond templated polymerizations, one sees little current evidence of real progress toward efficient synthesis of genuinely uniform chain populations. Nevertheless, recent advances in living ionic and metathesis polymerizations have been substantial and may in time lead to higher-order control of chain length, sequence, and stereochemistry. Issues such as environmental impact of the manufacture and disposal of polymers, along with the need for continuing improvement of cost/performance within the polymer industry, will cause polymer science to move in directions that will tend to minimize the numbers of monomers (raw materials) utilized by the industry and hence reduce the number of the chemistries presently in the waste stream. To achieve this, while preserving or expanding the current product diversity available with commercial polymers, increased interest in the effects of synthetic polymer primary specificity of structure of synthetic polymers on cost and performance will be manifest.

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Conclusions and Recon~ncr~ations 99 Cellular Synthesis of Materials It should be possible to develop cell "epitaxy" methods whereby biological cells are employed to fabricate thin layers (of organics or minerals) on synthetic material substrates, perhaps providing persistent maintenance and regulation as "epidermis." The objective is to use organisms as "microengineers" for structuring materials on difficult-to-manage length scales and with difficult-to-synthesize chemistries. The cellular mechanism is capable of organizing fibrous networks, for instance, with functional hydrogel components to produce low-friction, durable, fatigue-resistant joint bearings. Cellular responses to environmental effecters such as mechanical stress or hormones can beneficially change the composition and assembly of these materials. This is enabled through the coupling of specific protein synthesis and degradation with the constant monitoring of mechanical function and the state of need of the organism. Long- term cellular activity within the material can enable the repair of the material upon damage by reactivation of matrix formation. Not only could these advances create new membrane and biomaterial technologies but also new insights for structuring hard materials. Rigid Structural Composites Many of the rigid structural materials found in nature are composites that make up unusual compositions and configurations. For example, the nacreous material in mollusk shell is a segmented composite with a very low volume fraction of matrix phase in very thin layers. The ability to design and fabricate synthetic structures with similar characteristics, as well as the ability to mimic adhesion between the phases, could lead to composites with remarkable properties, by combining outstanding strength and stiffness with improved fracture toughness compared with that of monolithic materials. In addition to practical and cost-effective fabrication techniques, an understanding of deformation mechanisms and the

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loo Hierarchical Structures in Biology as a Guide for New Alatenals Technology ability to optimize composite structures through mechanical modeling are critical to the successful development of such materials. Adhesives and Interfaces Adhesives and interfaces play important roles in both synthetic and natural composites. Although much has been done in adhesion science and technology, there are opportunities to tailor new synthetic adhesives and unique structural architectures through mimicry of natural systems. Adhesives play a critical role in the formation, strength, and durability of composite materials as agents responsible for bonding between matrix and reinforcing phases. Advances in composites have emphasized the need for durable adhesives that would work in wet environments. Adhesives produced by organisms, especially marine organisms, suggest themselves as candidates for study, because they cure in the presence of water and resist its subversive effects. Naturally occurring marine adhesives are analogous to composite thermosets in that they are made up of fiber, filler, and catalyst molecules dispersed in a cross-linked resin. Resin proteins display a regular, repetitive structure that is thought to be related to their function (Waite, 1990~. For example, the East Coast blue mussel (Mytilus edulis) uses a resin polymer made up of approximately 80 repeats of a decamer. The West Coast mussel (Mytilus californianus) has evolved in an environment with greater wave action than the East Coast mussel and has resin virtually identical in structure except that two residues have been interchanged and a serine has been replaced by a threonine, a very conservative exchange. This small change in structure, however, produces an adhesive that is two to three times stronger than the East Coast adhesive (Waite, 1986~. This observation lends support to the view that mussel adhesive might be used as a model to systematically investigate the relationship between molecular structure and adhesive function, which could lead ultimately to a generic glue that can be modified at the molecular workbench for any number of different moist environments. If broad application is to be

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Conclusions and Recommendatwns 101 realized for such adhesives, however, functional durability over a wider range of temperatures must be achieved. Soft-Tissue-Based Materials Nature has developed exceptional designs for "ultrasoft" materials and for interfacing soft and hard materials with capabilities well beyond present day technology. Exposing the physical and chemical principles that underlie the special features of these materials is certain to stimulate new approaches to design of synthetic materials, parts, and systems. Therefore, the challenges are to extract design lessons from nature especially for development of material technologies that are inaccessible at present. These challenges include preparation of "self-healing" capsular materials that possess tunable and "motile" properties; methods for assembly of soft organic and hard material interfaces that are mechanically, chemically, and electrically compatible; and development of membrane composites that are based on fluid-surfactant interfaces that are supported by tethered polymer networks that possess permeability restriction and mechanical strength. An example of the potential impact of soft-tissue understanding is the reduction in energy needled to move a body through water when its drag is reduced. Also, in order to prevent detection, there is interest in reducing the hydrodynamic noise a body makes moving through water. Turbulence caused by a moving hull raises drag and hydrodynamic noise. There is no theory at present that links the viscoelastic properties of the surface of a body to its drag or its ability to reduce the amount of hull surface that causes turbulence. Dolphins have a peculiar skin overlying blubber and a collagenous subdermal sheath, and each of these tissue layers has different elastic and damping properties. More importantly, dolphins swim faster and farther using less metabolic energy than calculations would lead one to expect, and it is not clear how they do it. Further studies of the control of damping properties by the micro-, ultra-, and molecular structure of skin, blubber, and peripheral connective tissues of dolphins and of the boundary-layer conditions over their swimming

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102 Hierarchical strictures in Biology as a Guide for New lldaterials Technology bodies could lead to new methods for reducing turbulence, drag, and noise. A second soft tissue is muscle, a soft tissue that has no clear synthetic analogue. It is a transducer, converting electrical signals and chemical energy into mechanical motion. The characteristics of interest are response time, power density in terms of force developed per gram of muscle, and efficiency of power conversion. Piezoelectric transducers can do a similar job but give quite small motions for large applied voltages. Generally, engineers and designers must resort to small electric motors when building, for example, the arms for robots. Water-swollen cross-linked polymer gels can respond to electric fields by contracting in a way that is superficially similar to muscle. The field drives out a mobile counter-ion. The resulting neutralization of acid groups in the gel causes contraction. Devices have been made with these gels, but the response is slow (1-10 seconds compared with 10-100 milliseconds for muscle), and the power density is low. A soft, light, powerful actuator would have many applications in mechanical engineering ranging from actuators to engines. Intriguing progress toward these objectives has been reported (Urry et al., 1992~. Control of Size and Shape (Assembly, Self-Assembly) Inherent in the behavior of natural proteins is their assembly into structures of a given size and shape to allow the performance of a specific end-use function. This formation of parts and systems is driven by local geometry anti molecular forces and does not require additional "shaping and machining" steps. The ability to design synthetic systems capable of assembling in an analogous fashion would have obvious practical impact. For the purpose of this report, the determination of shape in biological systems needs to be considered at the level of hierarchical matrix formation. This is between the level of the component macromolecules, whose shapes determine their possible hierarchical interactions, and the level of whole cells, which appear almost

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Conclusions arid Recommendations 103 shapeless after isolation from their attachments to other cells and to adjacent extracellular matrix. Although the shape of an industrially produced article is defined by a set of dimensions that is measured with an externally applied scale, biological shape is determined by the history of internal manufacture of the object, as described in Chapter 2. A hallmark of biological matrix formation is the interaction beween matrix and the cell that adheres to it while manufacturing more of the same material. Previously it was mentioned that cells can be bioengineered to produce and secrete specific macromolecules. Up to now such cells, usually bacteria, yeasts, or insect cells, have been grown in suspension culture, without any specific orientation. For example, the previously mentioned bacteria that secrete cellulose are grown in suspension culture, which produces a random tangle of cellulose fibrils. However, if such cells were provided with cell surface receptors that attach to cellulose, then they could initially orient by attaching to previously made cellulose fibers. Their matrix production would thereby become vectorial with respect to the substrate to which they attach. The initial substrate that is provided to the cells could be structured by weaving, knitting, etc., and the subsequent matrix would be built on to that. The activities of the attached cells could be modulated in various ways, for example, to suppress or enhance cell replication locally and thereby produce patterns of increased concentrations of manufacturing cells. Cells have been engineered to express new receptors at their surfaces by inserting suitable genetic information into them. Furthermore, composite materials could be produced by replacing the initial manufacturing cells later by another set that have been engineered to produce a different matrix macromolecule. It was previously noted that biological shape emerges partly due to local sculpting. Highly controlled enzymes, such as some collagenases, and their inhibitors, are secreted by cells for limited, local and short-lived action. These enzymes may only modify their substrate, rather than totally destroy it. Limited etching, removal of material, is well established in the manufacture of microelectronic

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104 Hierarchical Stn~ca~res ir' Biology as a Guide for New Afatenals Technology devices and might have its counterpart in the above scheme of vectorial matrix production. Some natural self-assembling systems have a defined size, such as some vesicles, while other self-assembling systems are indefinite in extent, such as unstrained crystals. Proper function requires that system size be controlled as well as system shape. Some examples of methods to control and limit growth are . controlling the amount of material available for the transformation (the control mechanism is a time- dependent chemical potential); controlling the molecular geometry of vesicles; termination, due to build up of strain, of synthesis reactions within the molecule being created; and diffusion limited aggregation. The successful translation of these principles to synthetic materials could lead to the integration of the materials synthesis and processing steps of part fabrication. TECHNOLOGICAL OPPORTUNITIES Biomedical Materials There is a recognized societal and economic need for synthetic hierarchical materials with appropriate mechanical and functional performance characteristic properties for use in biomedical applications. This need represents a motivating opportunity for the scientific community to develop these materials. A brief summary of articular cartilage and diarthrodial joints has been presented (see Chapter 2) as a paradigm for hierarchical materials and structures with nanoscale, ultrascale, microscale, tissue-scale, and macroscale features that enable the performance critical to function. Nanoscale structures such as the charged groups

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Conclusions arid Recomm~ndanons 105 on the proteoglycan molecules provide the electrochemical bases for Donnan osmotic pressure and charge-to-charge repulsion. Ultrascale structures of proteoglycan aggregates and the collagen network provide the organization for the microporous solid matrix and its essential material properties. Microscale structures include specific cell types (chondrocytes), pericellular, territorial, and interterritorial extracellular matrix organization. These cells manufacture and organize the molecular building blocks and maintain the collagen-proteglycan extracellular solid matrix around themselves by a slow but balanced metabolic process. At the tissue-scale, articular cartilage possesses a set of unique nonlinear, anisotropic and nonhomogeneous material properties that seem to have been specifically designed to provide excellent long-term tribiological (friction, lubrication, and wear) functions at extremely high loads. Finally, at the macroscale, articular cartilage is the bearing material that provides the smooth, near frictionless function required of diarthrodial joints. The challenges in developing a manufacturing process to produce synthetic hierarchical materials with these required mechanical properties and functional characteristics are great. First, articular cartilage and other biologic tissues have very complex compositional make-ups and ultrastructural organizations. Second, the tissue is manufactured by tissue-specific cells in-situ. These cells are regulated by as yet unknown control processes, which control the production and assembly of the biomacromolecules and organize these macromolecules into an exquisite fabric that is the tissue. It is unlikely that any synthetic process can be developed in the near future that will duplicate the ability of the specific cells to manufacture and organize a hierarchical material with such fine ultrastructural features. However, a hybrid approach has been taken by some researchers, where synthetic grafts have been produced that are made of biocompatible resorbable matrices such as polylactic acid or copolymers of lactic and glycolic acids. These grafts serve as scaffolds for the specifically seeded cells (Cima et al., 1991~. These synthetic matrices are not subject to immune reactions. Other gels made of collagen and glycosaminoglycan seeded with cells also show promise

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106 Hierarchical Stn~ca~res in Biology as a Guide for New Materials Tecl~logy as graft materials for skin and blood vessels. However, for most gels currently available (e.g., fibrin clot that is used for joint surface repair), the material properties are probably insufficient for use in diarthrodial joints where the applied stresses are very high. Development of strong, cohesive, porous, permeable, resorbable gels that are capable of sustaining high stresses and strains and of providing a supporting and protecting environment for the seeded cells is a major challenge for future biomedical researchers interested in developing synthetic hierarchical materials for clinical use. Improved Membranes and Membrane-based Devices Improved membrane selectivity is desirable in the areas of water purification, protective clothing for those handling hazardous materials, outdoor clothing and shelters, gas separations, industrial purification processes, etc. Coupled with this is a need for improved stability and increased lifetime for these membranes and mechanisms, in order to reduce fouling. One approach to solving these problems is to incorporate responsive channels and self-repair ("living membranes") or self-cleaning attributes that are patterned after natural membrane systems. For a better understanding of membrane structures in terms of processing and assembly, the incorporation of responsive channels is key. Additional questions lie in the realm of suitable substitutes for water as plasticizers in these materials and in approaches to biomimetic membrane design. Smart Materials Natural systems have the ability to sense their surroundings and to respond to impulses or changes in conditions by changing properties or initiating self-preservation or repair responses. The development of smart materials, which integrate the functions of sensing, actuation, and control, can benefit greatly from lessons gleaned from the studies of these biological systems (Rogers, 1992~. Passively smart materials

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Conclusions and Recommendations 107 respond to external change without assistance, often through phase changes or transitions in fundamental properties. Actively smart materials utilize feedback loops to recognize changes and initiate appropriate responses (Newnham and Ruschau, 1990; Newnham, 1993). Opportunities for application of smart materials systems in structural applications generally focus on reduced component mass and adaptive functionality aimed at improving structural efficiency, durability, and safety. Examples of smart materials applications include load and vibration alleviation systems, failure sensing and repair, and shape memory. Challenges in sensor development and integration of sensing and response functions with practical structures need to be addressed to realize the potential of smart materials (NRC, 1 994). For example, important lessons can be learned by studying how sea urchins control the material properties of their bodies as a function of the local environment. Sea stars, sea urchins, and sea cucumbers (in fact, all echinoderms) can control the viscosity of their body wall and other connective tissues. Such tissues can be stiff enough to act as ligaments at one moment and undergo 30 percent extension the next. The change in stiffness and extension is reversible but not elastic, and an animal can cycle through these different states of stiffness-and- compliance, stretching-and-recovery dozens of times a day throughout its multiyear life without the materials showing wear or fatigue. The viscosity of the tissue is modulated by divalent cations, chiefly calcium, which form labile links in a mixture of collagen and glycoprotein molecules. A ganglion of nerve cell bodies whose long fingerlike processes (axons) carry chemicals to all parts of the ligament sits on each ligament. Thus, an important aspect of "smart materials" is sensing. In the case of echinoderms, these biological sensors (receptors) detect neurotransmitters from the nerve cells and in response allow a local increase in the concentration of divalent cations. An interesting class of nonbiological sensors is that of membranes or thin films adsorbed onto a surface. The chemical sensor consists of arrays of these films or membranes, each sensitive to different materials. There is every expectation that these sensors can

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108 Hierarchical Stn~c~rcs in Biology as a Guide for New Afatenals Technology be made with architectures similar to those of presently available microchips, with competitive cost/performance characteristics. Functionally Gradient Materials Functionally gradient materials (FGM) are defined as materials in which a continuous spatial change in composition or microstructure gives rise to position-dependent physical and mechanical properties that can extend over microscopic or macroscopic distances (Ramesh and Markworth, 1993~. Natural materials with functional gradients abound. Examples of materials with functional gradients that are discussed in this report include articular cartilage and bone. FGM can result in changes or orientation of constituents. For example, articular cartilage exhibits gradients in collagen/proteoglycan concentrations and in collagen fiber orientation. Often, as with cartilage, FGMs are used to provide an interracial transition between dissimilar materials or to provide multiple functions. Synthetic FGMs can be produced from mixtures of metals, polymers or ceramics in virtually any combination. A large part of the research in FGMs has focused on coatings and transitions for high- temperature aerospace applications like hypersonic aircraft and advanced turbine engines (Perepezko, 1991; Ramesh and Markworth, 1993~. Generally these systems transition from high-temperature resistant ceramics to metallic structural alloys. FGMs have been produced using vapor-phase synthesis, powder techniques, thermal spray processes, and self-propagating high-temperature synthesis. Another interesting area of research is surface gradients, where the nature of the surface is varied continuously with position (Elwing and Golander, 1991~. Gradients in surface areas have been produced that cause water to move uphill (Chaubhury and Whitesides, 1992~. Surface gradient techniques may find applications in processing, which will allow selective deposition or coating processes, or in tailored membrane or sensor applications. The development of functionally gradient materials is still in its early stages. The biggest challenge is in scaling the processes to

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Conclusions and Recomm~ndanons 109 practical size components while maintaining the precise control and consistency needed. The study of gradients in natural materials may provide direction for architectural design, fabrication processes, and potential applications for FGMs. Design and Assembly of Complex Composite Parts Competitive composite parts require three structural elements to be controlled in a manner that leads to a finished part that possesses the desired mechanical, thermal, and environmental properties in three dimensions. These elements are matrix uniformity, fiber orientation, and fiber-matrix surface interaction. Current methodologies are highly labor intensive, are not amenable to complex shape formation, and present significant problems in performance assessment. Often, machining, polishing, etc., is necessary to achieve the finished part shape and surface characteristics required for the application. In contrast, biological systems often contain complex and sophisticated fiber-reinforced composite "parts" examples range from trees to bones), which exhibit superb performance over extended lifetimes, are capable of healing, and are produced directly as finished parts from cell-based manufacturing plants. It is instructive to compare the "steps" of synthetic and biological fabrication technologies. SYNTHETIC BIOLOGICAL Produce Reinforcing Fiber Treat Fiber Surface Impregnate Fiber with Matrix Line Up Prepeg Plies in Mold Cure/Shane Part Produce Matrix "Scaffold" for Part Form Crystal Directing Surface Fill with "Gel" Replace Gel with Oriented "Fiber"

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llo Hierarchical Structures in Biology as a Guide for New Materials Technology In both cases, the materials employed and the final composite structure will contain key hierarchical structural elements. In the natural system, however, the hierarchy is a key to performance. Understanding and, where appropriate, mimicking the structure and manufacturing logic of natural hierarchies offer an opportunity to leapfrog current composite technologies and realize the promise of synthetic composites, which has proven elusive to the materials community for more than two decades. The toughest materials are known to raise the energy required for tearing by diverting cracks away from their preferred directions of propagation. A horse's hoof is difficult to split vertically (in the direction up the horse's leg). Hoof material contains keratin (the major protein in hair, finger nails, feathers, and rhino horn) in an ordered three-dimensional array such that a crack initiated by a vertical cut will turn and split the material at right angles to the vertical direction (circumferentially in the hoof). As a result, if a split does occur, it will cause the loss of a thin strip of the hoofs three- dimensional fiber array. The relationships between the array and the resistance to impact and control of crack propagation could illustrate new mechanisms of fracture toughness to be used in designing new synthetic materials. In addition, study of the mechanisms of synthesis of hoof material in the horse can be expected to provide hints for the industrial fabrication of such complex three-dimensional fibrous materials. However, improvements over current analysis methods are needed to take full advantage of these toughening mechanisms.