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1 INTRODUCTION Biological materials, such as tendon, bone, wood, and many others, are characterized by hierarchical architectural designs in which organization is controlled with striking precision on many discrete length scales, which range from the molecular to the macroscopic. These hierarchically structured materials display properties that are affected by processes operating at all levels of the length-scale spectrum. Most such materials are multifunctional and are produced in situ at room temperature and atmospheric pressure through ecologically balanced processes. Many are self-healing and thus remarkably durable even under high cyclic loading (e.g., a human knee joint), and many display properties that change, either abruptly or gradually, in response to a changing environment. Equipped to prepare only limited sets of constituent materials, organisms have evolved an astonishing array of architectural strategies to realize a broad range of structure and function. Virtually all biological materials are bounded systems that are synthesized and processed by cells at the nanoscale. Nature makes very different systems out of similar macromolecular and inorganic constituents through the process of differentiation during development. All of these materials systems have specific hierarchical composite structures. Starting with very similar macromolecular designs, each system (e.g., tendon, intestine, cornea, bone, etc.) is assembled to serve distinct, highly specific functions. These natural systems follow three rules for complex assemblies (Beer et al., 1992~. First, the structure is organized in discrete levels 13
14 Hierarchical Sauctures in Biology as a Guide for New Aiatenals Technology or scales. Virtually all biocomposite systems are found to have at least one distinct structural level at each of the molecular, nanoscopic, microscopic, and macroscopic scales. Second, the levels of structural organization are held together by specific interactions between components. Considerable evidence indicates that strong surface-to-surface interactions occur, which are caused by intermolecular covalent bonds at specific active sites or by strong van der Waals forces. Whatever the nature of the bonding between levels, adequate adhesion is required for system structural integrity. Finally, these highly interacting levels are organized into an oriented hierarchical composite system that is designed to meet a complex spectrum of functional requirements. Furthermore, as composite systems increase in complexity, they can function at higher levels of performance. The so-called intelligent materials and adaptive composite systems result from this type of complex architectural arrangement. A hierarchical biocomposite is more than just a material out of which larger objects can be built; it is a complete structural system in itself. Synthetic materials must be described in different terms. Free of the constraints imposed by biosynthetic pathways, materials scientists and engineers have created entirely new classes of metals, ceramics, polymers, and electronic materials with extraordinary properties. Nevertheless, many desirable features of biological materials have not yet been attained in synthetic systems. For example, synthetic materials may perform well with respect to a single figure of merit (e.g., strength) but fail to meet a more complex set of performance requirements that may include permeability, optical clarity, or frictional properties. Many synthetic materials must be processed at elevated temperatures and pressures or with the aid of environmentally burdensome organic solvents. In addition, self- healing materials and materials capable of controlled environmental response remain elusive. This situation has prompted growing interest within the materials community in the lessons that might be gleaned from a careful study of biological structures and of the processes by which
Introduction' 15 they are made. At the same time, biologists have begun to bridge the materials-biology gap through the application of increasingly powerful engineering analyses of natural structures and through the direct use of organisms to make interesting new materials or their building blocks. This report focuses on a ubiquitous feature of biological materials systems their hierarchical architectural design. What are the advantages of biological materials that are organized on many different length scales? What mechanical properties emerge from such designs? How does the architecture relate to the fabrication of the structure by the organism? Can synthetic materials systems be made this way? If so, what advantages might be realized? At the request of the Department of Defense and the National Aeronautics and Space Administration, the National Materials Advisory Board convened the Committee on Synthetic Hierarchical Structures to examine these issues and to review techniques related to preparing hierarchical structures that possess useful and unusual physical properties and to assess the opportunities for these structures in civilian and military applications. Although a broad range of functions are represented in biological systems, the committee concentrated on structural material systems and their properties. The purpose of this study was to conduct case-studies by selecting natural material systems to be used as models for synthetic efforts; characterize properties, unusual characteristics, and potential end-use applications for these synthetic systems; review state-of-the- art synthetic techniques and processes for assembling synthetic hierarchical structures; and recommend research that will expedite the understanding of the complex phenomena involved, lead to increased coordination among disciplines, and provide direction for future activities in the field.