DOI: 10.1126/science.1116994, 1144 (2005);310 Science

George MayerRigid Biological Systems as Models for Synthetic Composites

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R E V I E W

Rigid Biological Systems as Models forSynthetic Composites

George Mayer

Advances that have been made in understanding the mechanisms underlying themechanical behavior of a number of biological materials (namely mollusk shells andsponge spicules) are discussed here. Attempts at biomimicry of the structure of anacreous layer of a mollusk shell have shown reasonable success. However, they haverevealed additional issues that must be addressed if new synthetic composite materialsthat are based on natural systems are to be constructed. Some of the importantadvantages and limitations of copying from nature are also described here.

Rigid biological materials, such as shells,bone, and sponge spicules, have been attractiveas models for synthetic structural compositesbecause of their unusual combinations ofmechanical properties, suchas strength, stiffness, andtoughness. A study by theNational Materials Adviso-ry Board (1) dealt with thebroad area of biology as aguide for new materialstechnology, and that studyhas been followed, in recentyears, by books and reportsof symposia on biomimicryand bio-inspired materialsEsuch as (2, 3)^. The subjectof bone and its structure andmechanics has been exten-sively treated in a compre-hensive work by Currey (4),and much work has alsobeen done on many otheraspects of bone, such as thecreation of both natural andsynthetic bioresorbable scaf-folding for repairs (5). Thebody of work on bone isextensive, and the subject ofthe mimicking of bone de-serves a separate review.Therefore, the present workdeals only with the mecha-nisms underlying toughen-ing in mollusk shells andsponge spicules.

Increasing attention hasbeen devoted, in the pastthree decades, to the me-chanical behavior of theshells of mollusks. Curreywas the first to describe the

unusual toughness possessed by mother-of-pearl, the structure of nacre (6), and the widediversity of structural morphologies that havebeen found in seashells (7) (Fig. 1).

A key work by Jackson, Vincent, andTurner (8) illustrated examples of the attractivecombination of properties associated withnacre, in comparison with those of synthetic

composites that had high volume percent (v/o)of ceramic phase, along with an organic minorphase as matrix. Two important features ofnacre that distinguished it from the others inthe study were the closely packed layeredarchitecture and the soft matrix (or minor)phase. Nacre was also half as tough in the drystate as in the wet state (a factor that will bediscussed in a subsequent section).

The attractive combinations of mechani-cal properties of many rigid biological ma-terials stem from the fact that they are hybrid

composites, consisting of avery small volume fraction oforganic components (on theorder of 1 to 5 v/o) surround-ing a ceramic phase. Thearchitecture of a nacreousstructure is shown schemat-ically in Fig. 2. Often, natu-ral rigid materials that arefound in the oceans have alarge preponderance (on theorder of 95 v/o) of a ceram-ic component, such as CaCO3

(mollusk shells) or SiO2

(spicules of sponges thatlive in cold waters), that hasshown very limited tough-ness when used in its mono-lithic form.

Generally, what hasbeen copied from naturefor building synthetic struc-tural composites has beenthe architectural configura-tions and the material char-acteristics rather than thespecific natural materialsthat were originally found.This approach has limita-tions. A complicating anddifficult issue has been theenormous potential prob-lem of copying architectur-al features that are found innature, at the micro andnano scales, into real, mac-roscale structural materialsat reasonable cost.

Coincidentally, at leasttwo of the structures shown in Fig. 1, thenacreous and crossed-lamellar, are seen,respectively, in the brick-and-mortar archi-tecture of many buildings and in plywood

Department of Materials Science and Engineering,University of Washington, Roberts Hall 335, Box352120, Seattle, WA 98195–2120, USA. E-mail:gmayer@u.washington.edu

Fig. 1. Scanning electron micrographs, at various magnifications, of the fracturesurfaces of various mollusk shell structures: (A) prismatic, (B) nacreous, (C) cross-lamellar, (D) foliated, and (E) homogeneous (7). [Used with permission of the Societyfor Experimental Biology]

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(albeit at a much different scale and withdifferent material components).

Mechanisms Underlying Resistance toFailure in Rigid Natural Materials:Mollusk ShellsIn considering the toughness of rigid biolog-ical composites, an interpretation of toughnessthat is different from that used for conven-tional structural materials should be used.In the latter case, fracture toughness has todo with resistance to the propagation ofcracks. This is generally measured using so-called R curves (measures of resistance tounstable crack propagation), under the as-sumption that crack propagation is fairlystable and linear. In the natural rigid com-posites that have been studied by myself andothers, crack propagation is far from linear,and toughness in those materials should bereinterpreted as how much energy can beabsorbed and dissipated before catastrophicfailure. A convenient measureof energy dissipation may beestimated from the area un-der the load-deflection curvein the bending of a beam ofthe material. This has com-plex meaning for compositeswith high v/o of ceramic phase,because mechanisms that in-clude various forms of fractureactually dissipate much ener-gy. In addition, those mech-anisms can be substantiallyassisted by the unusual proper-ties of the thin, tenacious or-ganic phases. The latter havebeen observed to elongateextensively both elasticallyand viscoelastically. Althoughmany of the processes forenergy dissipation in naturalmaterials involve the cre-ation of new surfaces, by no means is thatthe whole story. At least 10 mechanismshave been observed to contribute to energydissipation in mollusk shell materials. Theseare:

1. Creation of new surface area by frac-ture and delamination; multiple microcrack-ing is included here (9).

2. Crack diversion.3. Pull-out of the ceramic phase from the

minor organic component, perhaps aided byasperities (from mineral bridges) on theplatelet surfaces, which provide frictional re-sistance against pull-out of the platelets (10).

4. Hole formation at the ends of thedisplaced ceramic-phase elements (whichseems similar to stress-whitening in poly-mers) at larger deformations (11).

5. A high level of anchoring of theorganic adhesive phase.

6. Ligament or filament formation in the

organic phase, which is viscoelastic (12) aswell as highly resilient.

7. Crack bridging by ligaments of theorganic phase.

8. Unfolding of chains, breaking of crosslinks (13), and perhaps permanent reorientationof the organic phase during deformation.

9. Moisture has a substantial plasticizingeffect on proteinaceous layers, thus leadingto increases in the work required to causefracturing (8, 14).

10. Contributions of residual stresses toenergy absorption (15). This was observed ina shell where two different adjacent struc-tural forms were present in a multilayeredstructure.

How much energy could be dissipated byeach of these mechanisms, and under whatconditions (varying strain rates and temper-atures, for example) they would be parti-tioned and triggered to operate, are presentlyunknown.

We have studied the mechanisms thatcontrol the attractive combinations of strength,stiffness, and energy absorption in a nacreousshell structure and have attempted to buildsynthetic composites at engineering scales(16). The nacre structure, found in the shellof the red abalone Haliotis rufescens, was ourmodel. The important features of that struc-ture showed (i) the existence of a space-filling, layered, and segmented architectureon the micro and nano scales. As shownschematically in Fig. 2, this is a ‘‘brick-and-mortar’’ structure, with the bricks approximat-ing hexagonal and other multisided platelets(from the top view). (ii) The major constituentis a ceramic phase, CaCO3, of a high volumefraction, along with a thin, viscoelastic, andresilient organic constituent (consisting ofproteins and possibly other organic ma-terials). The thin layer of the minor constit-uent is termed the matrix; it encases the

ceramic component on all sides and showsgreat adherence to the ceramic phase.

Development of a BiomimeticSynthetic CompositeWe designed simplified synthetic segmentedcomposite beams, based on the brick-and-mortar structure shown in Fig. 2. Materialswere selected, and composites were built onthe macro scale. Although nacre has micro-and nanoscale features, macroscale struc-tures were justified by observations of themechanical behavior of a synthetic ceramic/organic segmented material that had beenproposed for use as armor and reported in(16). The stacking architecture of the seg-mented composite plates had also beenstudied (17).

In this effort, there were a number of in-teresting sidelights, which illustrate the diffi-culty of mimicking natural composites. Thefirst of these was that ceramic materials such as

CaCO3 and SiO2 are not nor-mally considered for compo-nents of structural composites,because their mechanical prop-erties are generally insuf-ficient for such purposes.Therefore, Al2O3 (or alumina),a ‘‘workhorse’’ structural ce-ramic, was chosen as the ce-ramic component for thesynthetic composite, whichwas patterned after a simplifiednacre architecture. The organiccomponent of nacre appearedto have the characteristics of agood adhesive. However, whena very strong adhesive, such asa silicone-based material, wasused and beams of alumina/silicone adhesive were built (insegmented fashion) for bendtests, cracks were found to

traverse across the thickness of the beam quiteeasily. What had actually been observed in thefailure of nacre was that the organic (adhesive)phase allowed for reasonable strength but alsowould delaminate and promote crack diver-sion, while exhibiting fibril formation duringlarge deformation as well as strong tenacity tothe ceramic substrate. The search for a suitablesynthetic adhesive with nacre-like behaviorwas assisted by advice from a leading com-mercial adhesives source (18).

A second problem was that conventionalmonolithic ceramics generally need to have avery smooth surface finish for good fracturestrength. On the other hand, a polished surfaceis normally not helpful for the bonding of anadhesive.

One of the important findings of theseexperiments was that there appeared to be amaximum critical level of the organic phasethat controlled energy dissipation. Exceeding

Fig. 2. Schematic diagram of nacreous structure. The organic thin film indicatedbetween the layers also covers all other surfaces of each structural unit.

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that level meant that energy dissipation de-creased (Fig. 3). Also, although layered ce-ramic composites with continuous layersshowed greater strength and stiffness, energydissipation was not as high as that shown bythe segmented composite with low organicadhesive content.

The important role of very thin layers incontrolling the energy dissipation in naturalceramic/organic composites has been a keyfinding. When the amount of the adhesiveconstituent is at a critical level, it appearsthat a multitude of mechanisms of energydissipation are triggered. On the other hand,when that v/o of adhesive is larger than acritical volume fraction, the available modesseem to be much more limited. It remains tobe seen whether a smaller amount of ad-hesive component in the composite wouldyield even greater levels of energy dissipa-tion. Also, it has not been determined howenergy is distributed and dissipated amongthe various mechanisms, such as the creationof new surfaces, crack bridging, ligamentformation, unfolding ofmolecular chains, chainscission, etc.

It should also be notedthat, normally, in the con-sideration of energy ab-sorption by a structure,the elastic contribution isrecovered and given backto the loading frame of thetesting machine. In thecase of these inorganic/organic systems, it is notyet known how much ener-gy is elastic and how muchis viscoelastic. However, inFig. 3, the extended rangeof the synthetic compositewith the low v/o of adhe-sive phase covers a muchlarger zone than do the other examples thatwere tested. It was therefore concluded thatthe energy dissipation in the former wasmuch greater than that shown by the lattercomposites.

During the past several years, severalinvestigators (19, 20) have claimed that con-tinuous structural laminates of certain ceramic/metallic or intermetallic/metallic compo-sites were biomimetic in their origins andwere related to the superior combinationsof mechanical properties that have beenshown by nacre. Although continuous lami-nated composites of those materials doexhibit attractive mechanical properties(and showed retardation of crack propaga-tion), they do not closely mimic the struc-tures of mollusks. There are several reasonswhy this is so: (i) There is no report ofligament formation in the ductile metalliclayers of such composites, and that may be

one of the key energy-absorbing mechanismsunderlying energy dissipation in nacreousstructures. (ii) There has been no sign ofcrack bridging by the metallic component.(iii) The layers in materials such as nacreare segmented, rather than continuous. (iv)There has been no reported indication ofvery large resilience in these synthetic con-tinuous composites, as is shown in naturalrigid systems.

Mechanisms of Mechanical Behaviorof Siliceous Sponge StructuresAnother class of interesting natural structuralcomposites can be found in the spicules ofHexactinellid sponges. Spicules are buildingcomponents of the supports and skeletons ofmany sponges. They can be either calcareousor siliceous. Observations reported by Leviet al. (21) on silica-based spicules of aMonorhaphis sponge generated great interestbecause of their combination of properties,namely toughness (the new definition asenergy dissipation applies here, also) com-

bined with stiffness, and resilience. A pencil-sized rod spicule, on the order of a meter inlength, could be bent into a circle withoutbreaking. When the load was released, thespicule recovered its original shape. Whenthe bending of the spicule rod was comparedwith that of a silica rod, the toughness of thespicule was found to be nearly an order ofmagnitude higher. What differentiated thestructure of the spicule rod from that of thesilica rod was the presence of concentric ringsthat were separated by very thin organic layers.The structure of a similar but smaller spongespicule is shown in Fig. 4. Layers of hydratedsilica were found to be separated by muchthinner organic layers. In the central core ofthe spicules (not shown in Fig. 4) is a squarecross-section of protein filament, about 1 mmon each side.

Similar to the case of nacre, thin, flexible,tenacious layers have been proposed as a

major underlying reason for the large energydissipation and resilience of the spicules(22). When fractured spicules were exam-ined, the layers were found to be quiteeffective diverters of cracks. The similarityof Hexactinellid spicules to nacre seems toextend to the presence of very thin layersof complex organic material, in this case,well-bonded to a hydrated (silicate glass)substrate. We have estimated the volumefraction of organic constituents, includingthe central core region, in the spicules ofEuplectella aspergillum to be on the orderof 2 to 3 v/o (23). However, in the case ofspicules, the cylindrical components appear tobe continuous rather than segmented alongtheir lengths. The mechanisms that contributeto the ability to absorb energy are expected tobe similar to those that have been observed innacreous structures, but do not include themechanisms that are related to segmentedstructures, such as the pull-out of platelets.

The central protein filaments of thespicules of a different species of siliceous

sponge (not layered) havebeen studied by Morseand colleagues (24) andtermed silicateins (for sil-ica proteins). Three dif-ferent silicatein subunitshave been characterized.These are thought to con-trol the growth and formof the subsequent silicadeposition. The central fil-ament of E. aspergillumremains to be character-ized and will likely yieldresults different from thoseof prior studies.

The initial observationsabout toughening in thestudy by Levi et al. wereborne out by studies on

other Hexactinellid sponge species (22, 25).We have examined the behavior of spiculesof E. aspergillum in bending and undertension and have found them to be muchtougher [that is, they dissipated much more(six to seven times more) energy during de-formation until final failure] than conven-tional glass fibers of similar sizes (23). Theskeleton of this sponge also appears to be atorsion-resistant structure, as discussed in therecent comprehensive paper on the structuralhierarchy in this system by Aizenberg et al.(26). Structure indeed appears to followfunction here. In fact, the weave that isfound in the E. aspergillum skeleton (with-out the helical collar of reinforcements) issimilar to glass windings such as those foundin modern woven glass/epoxy composites.At this point in time, no known attemptshave been made to copy these siliceousstructures.

Load

Displacement

Composites with continuous layers

Segmented composites 82 v/o ceramic

Segmented composites 89 v/o ceramic

Fig. 3. Schematic bend test results of laminated synthetic composites (17); the energydissipated is estimated from the area under each curve.

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Advantages and Disadvantagesof Copying from NatureThe first issue that inevitably arises in lookingat natural materials and structures is thequestion ‘‘are the systems optimized?’’ andthe answer is probably ‘‘yes and no.’’ No,because of the limitations in the choice ofelements (C, Ca, P, Si, H, O, etc.) and ionsthat are found in the particular naturalenvironment. We know that, for engineeringpurposes, we are able to select and usestronger and more durable materials forstructures, and we may need them to functionover much wider temperature regimes. On theother hand, we should recognize that naturalstructures are designed to survive in environ-ments that have restricted mechanical loads,fairly narrow temperature regimes, and so on.The living plant or animal that cannot adaptits structure and properties to those environ-ments or to changes in them does not survive.If environments change gradually over time,some biological structures may be able toadapt. In the search for survival, living sys-tems such as mollusks and sponges have usedsophisticated biomineralization mechanismsthat provide the organisms with hybrid struc-tures that exhibit attractive combinations ofstrength, stiffness, resilience, and energy-absorbing capabilities (27). Thus, the synthe-sis of elegant structures and unique interfacesoccurs under the relatively mild conditions(and with the right catalysts) that are found inthe ocean, rather than under the much moreharsh high-temperature processing that isnormally done, for example, to make glass.It should, however, be emphasized that theproteins that exist in siliceous structures inthe ocean would not survive processing atthe high temperatures that are generally usedto form glass.

The foregoing facts caution us not to expectthat the structures found in the oceans wouldsurvive in more extreme environments of tem-perature and under other conditions that are

outside of their operating en-velopes. Of importance forcreating rigid structural ma-terials, thus far, in the area ofbiomimicry, are two majorfindings. The first is applyingarchitectural lessons in build-ing new hybrid composites[this has also been noted re-cently by Currey (28)]. Fromthe work reported in (16), itappears that architecture isa governing factor, as well,in building new materials atdifferent length scales. Thesecond important finding isthat a number of mechanicalproperties (such as ductility,resilience, and the ability todissipate energy) are con-

trolled by the thin organic layers in a rigidnatural material such as nacre. These layers(including those found in sponges) are muchmore complex than the synthetic adhesivesthat have been used in the building of seg-mented composite beams.

Some years ago, Weiner, Traub, andParker proposed a model of the various con-stituents in the thin layers surrounding nacreplatelets (29), and researchers at the Univer-sity of California at Santa Barbara havecharacterized an organic adhesive fibrillarcomponent that is responsible for the largeextension in nacre (30). In H. rufescens,three protein components have been identi-fied and connected with various roles inbiomineralization. More recent work inBremen (31) has clarified the key role ofthe nacre protein perlucin in nucleating thegrowth of calcium carbonate crystals in themarine snail H. laevigata. Thus, seriouscomplexities and connections between thebiomineralization, mechanical behavior, andmechanics of the organic constituents in nat-ural rigid composites remain to be addressedand solved.

Other important factors that affect themech-anical properties of rigid biological materialsare that these materials are generally highlydirectional and also are beneficially affected bymoisture. Moisture contributes greatly to thedissipation of energy, through plasticization ofthe small volume of proteinaceous matrix.

The organic phases in these rigid naturalcomposite materials, whether calcium orsilicon-based, also show viscoelasticity. Thiscan be seen in the behavior of samples ofnacre that were subjected to bending but hadnot been taken to failure (16), from strain-rate sensitivity tests on spicules of E. as-pergillum (22), and from the work of Ji andGao (12).

Of immense significance, too, are featuresthat have been observed, but researchers havethus far been unable to replicate in synthetic

systems, such as the ability for self-repair andthe exceptional tenacity at interfaces.

References and Notes1. Hierarchical Structures in Biology as a Guide for New

Materials Technology, NMAB-464 (National MaterialsAdvisory Board, National Academy Press, Washington,DC, 1990).

2. Design and Nature, C. A. Brebbia, L. J. Sucharov, P.Pascolo, Eds. (WIT Press, Southampton, UK, 2002).

3. Biological and Bioinspired Materials and Devices, vol. 823of Materials Research Society Symposium Proceedings,J. Aizenberg et al., Eds. (Materials Research Society,Warrendale, PA, 2004).

4. J. D. Currey, Bones: Structure and Mechanics (Prince-ton Univ. Press, Princeton, NJ, 2002).

5. Y. Zhang, M. Ni, M. Zhang, B. Ratner, Tissue Eng. 9,337 (2003).

6. J. D. Currey, Proc. R. Soc. London Ser. B 196, 443 (1977).7. J. D. Currey, in Symposium XXX1V, The Mechanical

Properties of Biological Materials (Symposia of theSociety for Experimental Biology, Cambridge Univ.Press, Cambridge, 1980), pp. 75–97.

8. A. P. Jackson, J. F. V. Vincent, R. M. Turner, J. Mater.Sci. 25, 3173 (1991).

9. S. Kamat, X. Su, R. Ballarini, A. H. Heuer, Nature 405,1036 (2000).

10. A. G. Evans, Z. Suo, R. Z. Wang, M. Y. He, J. W.Hutchinson, J. Mater. Res. 16, 2475 (2001).

11. R. Z. Wang, Z. Suo, A. G. Evans, N. Yao, I. A. Aksay,J. Mater. Res. 16, 2485 (2001).

12. B. Ji, H. Gao, J. Mech. Phys. Sol. 52, 1963 (2004).13. Z. Tang, N. A. Kotov, S. Magonov, B. Ozturk, Nat.

Mater. 2, 413 (2003).14. N. M. Neves, J. F. Mano, Mater. Sci. Eng. C 25, 113

(2005).15. D. J. Scurr, S. J. Eichhorn, in Mechanical Properties of

Bioinspired and Biological Materials, vol. 844 ofMaterials Research Society Symposium Proceedings, C.Viney et al., Eds. (Materials Research Society, Warren-dale, PA, 2005), pp. 87–92.

16. G. Mayer, Mat. Sci. Eng. C, in press.17. B. M. Gruner, thesis, University of Washington, Seattle,

WA (2003).18. A. V. Pocius, 3M Company, personal communication

(March 2002).19. M. Sarikaya et al., in Proceedings of the American

Society for Composites, 5th Technical Conference(Technomic Press, Lancaster, PA, 1990), pp. 176–182.

20. K. S. Vecchio, J. Miner. Met. Mat. Soc. 57, 25 (2005).21. C. Levi et al., J. Mater. Sci. Lett. 8, 337 (1989).22. G. Mayer et al., in Mechanical Properties of Bioinspired

and Biological Materials, vol. 844 of Materials ResearchSociety Symposium Proceedings, C. Viney et al., Eds.(Materials Research Society, Warrendale, PA, 2005),pp. 79–86.

23. S. G. Walter, B. D. Flinn, G. Mayer, Mat. Sci. Eng. C,in press.

24. J. N. Cha et al., Proc. Natl. Acad. Sci. U.S.A. 96, 361(1999).

25. M. Sarikaya et al., J. Mater. Res. 16, 1420 (2001).26. J. Aizenberg et al., Science 309, 275 (2005).27. S. Mann, Biomineralization (Oxford Univ. Press, Oxford,

2001).28. J. D. Currey, Science 309, 253 (2005).29. S. Weiner, W. Traub, S. B. Parker, Philos. Trans. R.

Soc. London Ser. B 304, 425 (1984).30. B. L. Smith et al., Nature 399, 761 (1999).31. S. Blank et al., J. Microsc. 212, 280 (2003).32. M. Rodriguez, thesis, University of Washington, Seattle,

WA (2004).33. I wish to express my appreciation to my present and

former students who have helped enormously to study,identify, and elucidate the micromechanisms underlyingmechanical behavior in rigid natural systems. Also, mythanks go to E. Baer and A.Hiltner, who brought fresh newinsight into hierarchical structures in biological systems; tothe late Sid Diamond of the U.S. Department of Energy,who strongly encouraged and supported the ongoingsearch for tough ceramic materials; and to my wife, Jane,for her help and patience.

10.1126/science.1116994

Fig. 4. Scanning electron micrograph of fractured Hexactinellidsponge spicule, showing concentric ring structure (32).

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