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HIERARCHICAL STRUCTURES IN BIOLOGY AS A GUIDE FOR NEW MATERIALS TECHNOLOGY COMMITTEE ON SYNTHETIC HIERARCHICAL STRUCTURES NATIONAL MATERIALS ADVISORY BOARD COMMISSION ON ENGINEERING AND TECHNICAL SYSTEMS NATIONAL RESEARCH COUNCIL NMAB-464 NATIONAL ACADEMY PRESS Washington, D.C. 1994

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NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance. This report has been reviewed by a group other than the authors according to procedures approved by a Report Review Committee consisting of members of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. This study by the National Materials Advisory Board was conducted under Contract No. MDA 972-92-C-0028 with the U.S. Department of Defense and the National Aeronautics and Space Administration. Library of Congress Catalog Card Number 94-69232 International Standard Book Number 0-309-04638-6 Available in limited supply from: Additional copies are available for sale from: National Materials Advisory Board National Academy Press 2101 Constitution Avenue, NW 2101 Constitution Avenue, NW HA-262 Washington, D.C. 20418 202-334-3505 Box 285 Washington, D.C. 20055 800-624-6242 or 202-334-3313 (in the Washington Metropolitan Area) Copyright 1994 by the National Academy of Sciences. All rights reserved. Printed in the United States of America. Cover photograph: Scanning electron micrograph of the fracture surface of the wing cover of a Bessbeetle (Popilitls disjunctusJ. Courtesy of Steve Gunderson, University of Dayton Research Institute. Cover diagram: Structural hierarchy of cellulose in wood. Courtesy of D. Kaplan, U. S. Army.

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COMMITTEE ON SYNTHETIC HIERARCHICAL STRUCTURES DAVID A. TIRRELL, Chair, University of Massachusetts, Amherst ILHAN AKSAY, Princeton University, Princeton, New Jersey ERIC BAER, Case Western Reserve University, Cleveland, Ohio PAUL D. CALVERT, University of Arizona, Tucson JOSEPH CAPPELLO, Protein Polymer Technologies, San Diego, California EDMUND A. DIMARZIO, National Institute of Standards and Technology, Gaithersburg, Maryland EVAN A. EVANS, University of British Columbia, Vancouver JOHN FESSLER, University of California, Los Angeles JOHN D. HOFFMAN, The Johns Hopkins University, Baltimore, Maryland MICHAEL JAFFE, Hoechst Celanese Research Division, Summit, New Jersey GEORGE MAYER, University of Pittsburgh, Pittsburgh, Pennsylvania VAN C. MOW, Columbia-Presbyterian Medical Center, Columbia University, New York, New York STEPHEN A. WAINWRIGHT, Duke University, Durham, North Carolina Government Liaison Representatives ED CHEN, U.S. Army Laboratory Command, Army Research Office, Research Triangle Park, North Carolina FREDERICK L. HEDBERG, Air Force Office of Scientific Research, Washington, D.C. .

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DAVID KAPLAN, Department of the Army, Natick Research Development and Engineering Center, Natick, Massachusetts MICHAEL MARRON, Office of Naval Research, Arlington, Virginia IRA SKURNICK, Advance Research Projects Agency/Defense Sciences Office, Arlington, Virginia NORMAN TALLAN, Wright Patterson Air Force Base, Ohio RONALD TAYLOR, National Academy of Sciences, Washington, D.C. HOLLIS WICKMAN, National Science Foundation, Washington, D.C. National Materials Advisory Board Staff THOMAS E. MUNNS, Senior Program Officer AIDA C. NEEL, Senior Project Assistant 1V

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ACKNOWLEDGMENTS The Committee on Synthetic Hierarchical Structures is grateful to many individuals for their presentations covering specific technical areas relevant to hierarchical systems. Speakers included Dr. Richard Farrell and Mr. Russell McCalley of Johns Hopkins University's Applied Physics Laboratory, who discussed cornea structure and its effects on corneal transparency; Dr. Donald Johnson of Weyerhaeuser, who spoke of the production of bacterial cellulose; Dr. Clement Furlong of the University of Washington, who talked on the production of proteins for commercially useful self-assembly systems; and Dr. Robert Newnham of Pennsylvania State University, who discussed electroceramics, which included smart materials and biomimetics. The committee is also grateful to the government liaison representatives for their participation in a number of committee discussions in particular to Dr. David Kaplan of the U.S. Army's Natick Laboratory, who described some of the laboratory's in-house programs and interests in hierarchical systems and whose own research is reflected in these pages, and to Michael Marron of the Office of Naval Research, who identified needs in adhesive bonding. The chair of the committee thanks the members for their dedication and patience during the numerous iterations and revisions of the report. Finally, the committee gratefully acknowledges the support of Dr. Stanley Barkin, the senior program officer who supported the study until his retirement in April 1992; his successor, Mr. Thomas E. Munns; and administrative assistants, Ms. Cathryn Summers and Ms. Aida C. Neel. v

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The National Academy of Sciences is a private, nonprofit, self- perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Bruce M. Alberts is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Robert M. White is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Kenneth I. Shine is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy's purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government' the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Bruce M. Alberts and Dr. Robert M. White are chairman and vice chairman, respectively, of the National Research Council. . V1

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ABSTRACT Hierarchical structures are assemblages of molecular units or their aggregates that are embedded or intertwined with other phases, which in turn are similarly organized at increasing size levels. The multilevel architectures are capable of conferring unique properties to the structure. Hierarchical structures are found in practically all complex systems, particularly naturally occurring ones. Synthetic hierarchical structures can be prepared from metals, ceramics, or polymers, or from hybrids of various classes of these materials. The Committee on Synthetic Hierarchical Structures made an assessment of the opportunities to prepare hierarchical structures that possess useful and unusual physical properties for civilian and military applications. It conducted case-studies by selecting natural material systems to be used as models for synthetic efforts. It reviewed the state of the art of synthetic techniques and processes for assembling synthetic hierarchical structures. The committee also characterized properties, unusual characteristics, and potential end-use applications for these synthetic systems. Finally, the committee recommended research directions to expedite the understanding of the complex phenomena involved, lead to increased coordination among disciplines, and provide direction for future activities in the field. - V11

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PREFACE Many materials systems found in nature exhibit a combination of properties that is not found in synthetic systems. The unique performance of natural materials arises from precise hierarchical organization over a large range of length scales. These materials display unique properties that are affected by structure and generative processes at all levels of the biological structural hierarchy. At the request of the Department of Defense and the National Aeronautics and Space Administration, the National Materials Advisory Board convened a committee' the Committee on Synthetic Hierarchical Structures, to review techniques related to the preparation of hierarchical structures that possess useful and unusual physical properties and 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. The approach taken by the committee was to conduct case-studies that selected 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. In Chapter 1, the concept of hierarchical materials systems is introduced. Chapter 2 examines hierarchical architecture and illustrates its significance through a discussion of the structures and properties of a variety of biological materials systems. Several examples of synthetic hierarchical materials systems are described in . IX

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Chapter ]. Chapter 4 assesses the current capacl1y 10 produce such materials. And Chapter ~ presents the conclusions and recommendations of the committee, identifies grew of science sad technology where hierarchical materials systems could play important roles, and suggests the research objectives that must be met to realize the potential of this new approach to malerlab technology. David A. Tirrell Chair x

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CONTENTS EXECUTIVE SUMMARY 1 INTRODUCTION 2 NATURAL HIERARCHICAL MATERIALS Recurrent Use of Molecular Constituents, 18 Controlled Orientation, 23 Durable Interfaces Between Hard and Soft Materials, 26 The Role of Water, 27 Property Variation in Response to Changing Performance Requirements, 32 Fatigue Resistance and Self-Repair, 34 Shape Control, 36 3 SYNTHETIC HIERARCHICAL SYSTEMS Introduction, 39 One-Dimensional Hierarchy, 43 Two-Dimensional Hierarchy, 49 Three-Dimensional Hierarchy, 52 Adjustable Variables and Their Influence on Mechanical Behavior of Synthetic Materials, 59 4 FABRICATION OF HIERARCHICAL SYSTEMS Synthetic Processing, 75 Biologically Inspired Processing, 84 Xl 1 13 17 39 73

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CONCLUSIONS AND RECOH~ENDAlIONS: SCIENlIfIC AND TECHNOLOGICAL OPPORTUNITIES 93 rf~/~, P' frore~f",, ad " ~d at/ Pa "fNe~, Pa a// Oppor'""f4~, 704 REFERENCES APPENDIX ~ GLOSSARY OF leaks APPENDIX ~ BIOGRAPHICAL SKETCHES OF CO~HIllEE HEHHERS . . X11 111 123 127

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HIERARCHICAL STRUCTURES IN BIOLOGY AS A GUIDE FOR NEW MATERIALS TECHNOLOGY

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