Special Reviews

Rigid Biological Systems as Models for Synthetic Composites

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Science  18 Nov 2005:
Vol. 310, Issue 5751, pp. 1144-1147
DOI: 10.1126/science.1116994


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

Rigid biological materials, such as shells, bone, and sponge spicules, have been attractive as models for synthetic structural composites because of their unusual combinations of mechanical properties, such as strength, stiffness, and toughness. A study by the National Materials Advisory Board (1) dealt with the broad area of biology as a guide for new materials technology, and that study has been followed, in recent years, by books and reports of symposia on biomimicry and bio-inspired materials [such as (2, 3)]. The subject of bone and its structure and mechanics has been extensively treated in a comprehensive work by Currey (4), and much work has also been done on many other aspects of bone, such as the creation of both natural and synthetic bioresorbable scaffolding for repairs (5). The body of work on bone is extensive, and the subject of the mimicking of bone deserves a separate review. Therefore, the present work deals only with the mechanisms underlying toughening in mollusk shells and sponge spicules.

Increasing attention has been devoted, in the past three decades, to the mechanical behavior of the shells of mollusks. Currey was the first to describe the unusual toughness possessed by mother-of-pearl, the structure of nacre (6), and the wide diversity of structural morphologies that have been found in seashells (7) (Fig. 1).

Fig. 1.

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

A key work by Jackson, Vincent, and Turner (8) illustrated examples of the attractive combination of properties associated with nacre, in comparison with those of synthetic composites that had high volume percent (v/o) of ceramic phase, along with an organic minor phase as matrix. Two important features of nacre that distinguished it from the others in the study were the closely packed layered architecture and the soft matrix (or minor) phase. Nacre was also half as tough in the dry state as in the wet state (a factor that will be discussed in a subsequent section).

The attractive combinations of mechanical properties of many rigid biological materials stem from the fact that they are hybrid composites, consisting of a very small volume fraction of organic components (on the order of 1 to 5 v/o) surrounding a ceramic phase. The architecture of a nacreous structure is shown schematically in Fig. 2. Often, natural rigid materials that are found in the oceans have a large preponderance (on the order of 95 v/o) of a ceramic component, such as CaCO3 (mollusk shells) or SiO2 (spicules of sponges that live in cold waters), that has shown very limited toughness when used in its monolithic form.

Fig. 2.

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

Generally, what has been copied from nature for building synthetic structural composites has been the architectural configurations and the material characteristics rather than the specific natural materials that were originally found. This approach has limitations. A complicating and difficult issue has been the enormous potential problem of copying architectural features that are found in nature, at the micro and nano scales, into real, macroscale structural materials at reasonable cost.

Coincidentally, at least two of the structures shown in Fig. 1, the nacreous and crossed-lamellar, are seen, respectively, in the brick-and-mortar architecture of many buildings and in plywood (albeit at a much different scale and with different material components).

Mechanisms Underlying Resistance to Failure in Rigid Natural Materials: Mollusk Shells

In considering the toughness of rigid biological composites, an interpretation of toughness that is different from that used for conventional structural materials should be used. In the latter case, fracture toughness has to do with resistance to the propagation of cracks. This is generally measured using so-called R curves (measures of resistance to unstable crack propagation), under the assumption that crack propagation is fairly stable and linear. In the natural rigid composites that have been studied by myself and others, crack propagation is far from linear, and toughness in those materials should be reinterpreted as how much energy can be absorbed and dissipated before catastrophic failure. A convenient measure of energy dissipation may be estimated from the area under the load-deflection curve in the bending of a beam of the material. This has complex meaning for composites with high v/o of ceramic phase, because mechanisms that include various forms of fracture actually dissipate much energy. In addition, those mechanisms can be substantially assisted by the unusual properties of the thin, tenacious organic phases. The latter have been observed to elongate extensively both elastically and viscoelastically. Although many of the processes for energy dissipation in natural materials involve the creation of new surfaces, by no means is that the whole story. At least 10 mechanisms have been observed to contribute to energy dissipation in mollusk shell materials. These are:

  1. Creation of new surface area by fracture and delamination; multiple microcracking is included here (9).

  2. Crack diversion.

  3. Pull-out of the ceramic phase from the minor organic component, perhaps aided by asperities (from mineral bridges) on the platelet surfaces, which provide frictional resistance against pull-out of the platelets (10).

  4. Hole formation at the ends of the displaced ceramic-phase elements (which seems similar to stress-whitening in polymers) at larger deformations (11).

  5. A high level of anchoring of the organic adhesive phase.

  6. Ligament or filament formation in the organic phase, which is viscoelastic (12) as well as highly resilient.

  7. Crack bridging by ligaments of the organic phase.

  8. Unfolding of chains, breaking of cross links (13), and perhaps permanent reorientation of the organic phase during deformation.

  9. Moisture has a substantial plasticizing effect on proteinaceous layers, thus leading to increases in the work required to cause fracturing (8, 14).

  10. Contributions of residual stresses to energy absorption (15). This was observed in a shell where two different adjacent structural forms were present in a multilayered structure.

How much energy could be dissipated by each of these mechanisms, and under what conditions (varying strain rates and temperatures, for example) they would be partitioned and triggered to operate, are presently unknown.

We have studied the mechanisms that control the attractive combinations of strength, stiffness, and energy absorption in a nacreous shell structure and have attempted to build synthetic composites at engineering scales (16). The nacre structure, found in the shell of the red abalone Haliotis rufescens, was our model. The important features of that structure showed (i) the existence of a space-filling, layered, and segmented architecture on the micro and nano scales. As shown schematically in Fig. 2, this is a “brick-and-mortar” structure, with the bricks approximating hexagonal and other multisided platelets (from the top view). (ii) The major constituent is a ceramic phase, CaCO3, of a high volume fraction, along with a thin, viscoelastic, and resilient organic constituent (consisting of proteins and possibly other organic materials). The thin layer of the minor constituent is termed the matrix; it encases the ceramic component on all sides and shows great adherence to the ceramic phase.

Development of a Biomimetic Synthetic Composite

We designed simplified synthetic segmented composite beams, based on the brick-and-mortar structure shown in Fig. 2. Materials were selected, and composites were built on the macro scale. Although nacre has micro- and nanoscale features, macroscale structures were justified by observations of the mechanical behavior of a synthetic ceramic/organic segmented material that had been proposed for use as armor and reported in (16). The stacking architecture of the segmented composite plates had also been studied (17).

In this effort, there were a number of interesting sidelights, which illustrate the difficulty of mimicking natural composites. The first of these was that ceramic materials such as CaCO3 and SiO2 are not normally considered for components of structural composites, because their mechanical properties are generally insufficient for such purposes. Therefore, Al2O3 (or alumina), a “workhorse” structural ceramic, was chosen as the ceramic component for the synthetic composite, which was patterned after a simplified nacre architecture. The organic component of nacre appeared to have the characteristics of a good adhesive. However, when a very strong adhesive, such as a silicone-based material, was used and beams of alumina/silicone adhesive were built (in segmented fashion) for bend tests, cracks were found to traverse across the thickness of the beam quite easily. What had actually been observed in the failure of nacre was that the organic (adhesive) phase allowed for reasonable strength but also would delaminate and promote crack diversion, while exhibiting fibril formation during large deformation as well as strong tenacity to the ceramic substrate. The search for a suitable synthetic adhesive with nacre-like behavior was assisted by advice from a leading commercial adhesives source (18).

A second problem was that conventional monolithic ceramics generally need to have a very smooth surface finish for good fracture strength. On the other hand, a polished surface is normally not helpful for the bonding of an adhesive.

One of the important findings of these experiments was that there appeared to be a maximum critical level of the organic phase that controlled energy dissipation. Exceeding that level meant that energy dissipation decreased (Fig. 3). Also, although layered ceramic composites with continuous layers showed greater strength and stiffness, energy dissipation was not as high as that shown by the segmented composite with low organic adhesive content.

Fig. 3.

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

The important role of very thin layers in controlling the energy dissipation in natural ceramic/organic composites has been a key finding. When the amount of the adhesive constituent is at a critical level, it appears that a multitude of mechanisms of energy dissipation are triggered. On the other hand, when that v/o of adhesive is larger than a critical volume fraction, the available modes seem to be much more limited. It remains to be seen whether a smaller amount of adhesive component in the composite would yield even greater levels of energy dissipation. Also, it has not been determined how energy is distributed and dissipated among the various mechanisms, such as the creation of new surfaces, crack bridging, ligament formation, unfolding of molecular chains, chain scission, etc.

It should also be noted that, normally, in the consideration of energy absorption by a structure, the elastic contribution is recovered and given back to the loading frame of the testing machine. In the case of these inorganic/organic systems, it is not yet known how much energy is elastic and how much is viscoelastic. However, in Fig. 3, the extended range of the synthetic composite with the low v/o of adhesive phase covers a much larger zone than do the other examples that were tested. It was therefore concluded that the energy dissipation in the former was much greater than that shown by the latter composites.

During the past several years, several investigators (19, 20) have claimed that continuous structural laminates of certain ceramic/metallic or intermetallic/metallic composites were biomimetic in their origins and were related to the superior combinations of mechanical properties that have been shown by nacre. Although continuous laminated composites of those materials do exhibit attractive mechanical properties (and showed retardation of crack propagation), they do not closely mimic the structures of mollusks. There are several reasons why this is so: (i) There is no report of ligament formation in the ductile metallic layers of such composites, and that may be one of the key energy-absorbing mechanisms underlying energy dissipation in nacreous structures. (ii) There has been no sign of crack bridging by the metallic component. (iii) The layers in materials such as nacre are segmented, rather than continuous. (iv) There has been no reported indication of very large resilience in these synthetic continuous composites, as is shown in natural rigid systems.

Mechanisms of Mechanical Behavior of Siliceous Sponge Structures

Another class of interesting natural structural composites can be found in the spicules of Hexactinellid sponges. Spicules are building components of the supports and skeletons of many sponges. They can be either calcareous or siliceous. Observations reported by Levi et al. (21) on silica-based spicules of a Monorhaphis sponge generated great interest because of their combination of properties, namely toughness (the new definition as energy dissipation applies here, also) combined with stiffness, and resilience. A pencil-sized rod spicule, on the order of a meter in length, could be bent into a circle without breaking. When the load was released, the spicule recovered its original shape. When the bending of the spicule rod was compared with that of a silica rod, the toughness of the spicule was found to be nearly an order of magnitude higher. What differentiated the structure of the spicule rod from that of the silica rod was the presence of concentric rings thatwereseparatedbyverythinorganiclayers. The structure of a similar but smaller sponge spicule is shown in Fig. 4. Layers of hydrated silica were found to be separated by much thinner organic layers. In the central core of the spicules (not shown in Fig. 4) is a square cross-section of protein filament, about 1 μm on each side.

Fig. 4.

Scanning electron micrograph of fractured Hexactinellid sponge spicule, showing concentric ring structure (32).

Similar to the case of nacre, thin, flexible, tenacious layers have been proposed as a major underlying reason for the large energy dissipation and resilience of the spicules (22). When fractured spicules were examined, the layers were found to be quite effective diverters of cracks. The similarity of Hexactinellid spicules to nacre seems to extend to the presence of very thin layers of complex organic material, in this case, well-bonded to a hydrated (silicate glass) substrate. We have estimated the volume fraction of organic constituents, including the central core region, in the spicules of Euplectella aspergillum to be on the order of 2 to 3 v/o (23). However, in the case of spicules, the cylindrical components appear to be continuous rather than segmented along their lengths. The mechanisms that contribute to the ability to absorb energy are expected to be similar to those that have been observed in nacreous structures, but do not include the mechanisms that are related to segmented structures, such as the pull-out of platelets.

The central protein filaments of the spicules of a different species of siliceous sponge (not layered) have been studied by Morse and colleagues (24) and termed silicateins (for silica proteins). Three different silicatein subunits have been characterized. These are thought to control the growth and form of the subsequent silica deposition. The central filament of E. aspergillum remains to be characterized and will likely yield results different from those of prior studies.

The initial observations about toughening in the study by Levi et al. were borne out by studies on other Hexactinellid sponge species (22, 25). We have examined the behavior of spicules of E. aspergillum in bending and under tension and have found them to be much tougher [that is, they dissipated much more (six to seven times more) energy during deformation until final failure] than conventional glass fibers of similar sizes (23). The skeleton of this sponge also appears to be a torsion-resistant structure, as discussed in the recent comprehensive paper on the structural hierarchy in this system by Aizenberg et al. (26). Structure indeed appears to follow function here. In fact, the weave that is found in the E. aspergillum skeleton (without the helical collar of reinforcements) is similar to glass windings such as those found in modern woven glass/epoxy composites. At this point in time, no known attempts have been made to copy these siliceous structures.

Advantages and Disadvantages of Copying from Nature

The first issue that inevitably arises in looking at natural materials and structures is the question “are the systems optimized?” and the answer is probably “yes and no.” No, because of the limitations in the choice of elements (C, Ca, P, Si, H, O, etc.) and ions that are found in the particular natural environment. We know that, for engineering purposes, we are able to select and use stronger and more durable materials for structures, and we may need them to function over much wider temperature regimes. On the other hand, we should recognize that natural structures are designed to survive in environments that have restricted mechanical loads, fairly narrow temperature regimes, and so on. The living plant or animal that cannot adapt its structure and properties to those environments or to changes in them does not survive. If environments change gradually over time, some biological structures may be able to adapt. In the search for survival, living systems such as mollusks and sponges have used sophisticated biomineralization mechanisms that provide the organisms with hybrid structures that exhibit attractive combinations of strength, stiffness, resilience, and energy-absorbing capabilities (27). Thus, the synthesis of elegant structures and unique interfaces occurs under the relatively mild conditions (and with the right catalysts) that are found in the ocean, rather than under the much more harsh high-temperature processing that is normally done, for example, to make glass. It should, however, be emphasized that the proteins that exist in siliceous structures in the ocean would not survive processing at the high temperatures that are generally used to form glass.

The foregoing facts caution us not to expect that the structures found in the oceans would survive in more extreme environments of temperature and under other conditions that are outside of their operating envelopes. Of importance for creating rigid structural materials, thus far, in the area of biomimicry, are two major findings. The first is applying architectural lessons in building new hybrid composites [this has also been noted recently by Currey (28)]. From the work reported in (16), it appears that architecture is a governing factor, as well, in building new materials at different length scales. The second important finding is that a number of mechanical properties (such as ductility, resilience, and the ability to dissipate energy) are controlled by the thin organic layers in a rigid natural material such as nacre. These layers (including those found in sponges) are much more complex than the synthetic adhesives that have been used in the building of segmented composite beams.

Some years ago, Weiner, Traub, and Parker proposed a model of the various constituents in the thin layers surrounding nacre platelets (29), and researchers at the University of California at Santa Barbara have characterized an organic adhesive fibrillar component that is responsible for the large extension in nacre (30). In H. rufescens, three protein components have been identified and connected with various roles in biomineralization. More recent work in Bremen (31) has clarified the key role of the nacre protein perlucin in nucleating the growth of calcium carbonate crystals in the marine snail H. laevigata. Thus, serious complexities and connections between the biomineralization, mechanical behavior, and mechanics of the organic constituents in natural rigid composites remain to be addressed and solved.

Other important factors that affect the mechanical properties of rigid biological materials are that these materials are generally highly directional and also are beneficially affected by moisture. Moisture contributes greatly to the dissipation of energy, through plasticization of the small volume of proteinaceous matrix.

The organic phases in these rigid natural composite materials, whether calcium or silicon-based, also show viscoelasticity. This can be seen in the behavior of samples of nacre that were subjected to bending but had not been taken to failure (16), from strainrate sensitivity tests on spicules of E. aspergillum (22), and from the work of Ji and Gao (12).

Of immense significance, too, are features that have been observed, but researchers have thus far been unable to replicate in synthetic systems, such as the ability for self-repair and the exceptional tenacity at interfaces.

References and Notes

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