PerspectiveMaterials Science

Hierarchies in Biomineral Structures

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Science  08 Jul 2005:
Vol. 309, Issue 5732, pp. 253-254
DOI: 10.1126/science.1113954

Most animals mineralize at least part of their bodies, usually for skeletal support. Various minerals are used, with calcium carbonate, silica (glass), and calcium phosphate being the most common. Despite this diversity of materials, there is one nearly constant feature: Almost all biomineralized structures are highly hierarchical, that is, the structure is different at many different length scales. On page 275 of this issue, Aizenberg et al. (1) show how the glassy sponge Euplectella, which uses silica as its skeletal building block, makes a skeleton of extraordinary structural and mechanical refinement with many levels of hierarchy.

Euplectella is a deepwater sponge whose glassy skeleton is a hollow cylinder. On the first level of structural hierarchy, nanometer-sized particles of silica are arranged around an organic axial filament. On the second level, alternating layers of silica and organic material form spicules. On the third level, these small spicules are bundled together to form larger spicules. On the fourth level, the larger spicules are arranged in a grid, with struts in longitudinal, circumferential, and diagonal directions, resisting all load modes (see the figure). In the mature animal, these larger spicules are coated with a cementing layer of silica. On the fifth level, this grid is wrapped into a curved cylinder. Finally, on the sixth level, helical surface ridges further resist torsion and stiffen the structure (2).

The precise mechanical consequences of the arrangement of the Euplectella skeleton have yet to be worked out in detail, but most are self-evident. Perhaps the most remarkable feature of this skeleton is at level four. Theoretical analysis by Deshpande et al. (3) has shown that mass and metabolic effort can be minimized for a given stiffness by having anti-shear diagonal struts in every other square. This is the pattern shown by Euplectella (see the figure, left and middle panels).

How to resist loads.

(Left) Arrangement of a square network that is stiff in shear, even though half the cells are not stiffened. [Modified from (3)] (Middle) In the Euplectella skeleton, only half the squares are crossed by shear-stiffening fibers. The sides of the squares are ~3 mm long. (Right) Microradiograph of a section of the head of a human femur (9), showing the cortical bone (solid black around the outside) and the trabecular bone inside. The direction of the bony trabeculae is related to the direction of the loads on the bone during walking.

CREDIT: (MIDDLE) J. D. CURREY. (RIGHT) REPRINTED FROM (9) WITH PERMISSION FROM ELSEVIER

The structural complexity of the Euplectella skeleton is not quite matched by other skeletons, but the characteristic hierarchy is. In a mammalian bone, at the lowest level, nanometer-sized crystals of carbonate apatite are embedded in, and surround, the fibrous protein collagen. At the next level, these mineralized fibers lie bundled together and attached to each other. At the next level, these fibers come together to form lamellae with a width of ~2 μm. The lamellae have various patterns; a very common one is a secondary osteon, in which concentric lamellae form cylindrical structures, ~200 μm in diameter, surrounding a central blood vessel. Compact bone, solid to the naked eye, is modified in places to form trabecular bone, which consists of many struts; the spaces between the struts are filled with marrow (see the figure, right panel). These struts are not randomly arranged, but are related to the direction of loads on the bone. The mechanical and other properties of bone depend on the interaction of all levels of organization (4).

Two more examples of the structural hierarchy of biominerals are the teeth of sea urchins and the “crossed-lamellar” structure of many mollusk shells. The crossed-lamellar structure consists almost entirely of calcium carbonate in the crystalline form of aragonite, with a tiny amount of organic material between the crystals. It has five levels of organization, and the structures are arranged with high precision to prevent the traveling of cracks (5, 6). Sea urchin teeth have fewer levels of hierarchy, but their structure is very similar to that of fiber-reinforced plastics. However, they consist of a composite in which fibers and matrix are chemically identical, being made of calcite, although the crystals differ greatly in size and orientation, with a layer of organic material surrounding the fibers (7). Furthermore, the magnesium content of the calcite increases toward the middle of the tooth, markedly increasing its hardness. The resulting differential wear produces a self-sharpened tooth.

The main mechanical function of these hierarchical arrangements, almost certainly, is to produce interfaces that will open up in the presence of potentially dangerous cracks, deflecting the cracks and making their travel energetically expensive. This makes biomineralized skeletons surprisingly tough, given that they are made almost entirely of mineral. Bone is a special case, having less mineral than most other biomineralized skeletons; it can be remarkably tough.

Apart from their hierarchical arrangement, two other features of biominerals contribute to the superior mechanical properties of skeletons made from them. First, at the lowest level, they are often made of tiny crystals that are smaller than the “Griffith length” necessary for cracks to spread (8). Second, the precision with which they can be laid down (changing their main orientation over a few micrometers, for instance) allows exquisite adaptations to the loads falling on the skeletons.

The particular mineral used in a skeleton—calcite, aragonite, apatite, silica, or others—is probably much less important than the precise way in which the mineral is arranged in space. Aizenberg et al. show this very clearly for the Euplectella skeleton, although the organic component is also crucial for providing clear interfaces between the layers.

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