The many adaptations of bone
Introduction
The ability of a bone to function effectively under the loads that are imposed on it depends upon two factors: the properties of the bone material, and arrangement of this material in space—the size and shape of the bone. Most experiments and theory about bone adaptation are concerned with the latter, with the placing or replacing of bony mass. This is usually termed ‘modelling’ and is produced by the probably rather uncoordinated activity of bone cells. It should be distinguished from ‘remodelling’ which is also a matter of lively concern, particularly where it occurs in cancellous bone, in which osteoclasts and osteoblasts work together in a coordinated sequence to replace bone and usually leave the total amount of bone unaltered, in the form of secondary osteones (Haversian systems). There has been much less concern about the other adaptations that bone may have; in particular there has been little consideration of how bone material properties may be related to the loads falling on the bone. This review surveys some aspects of this subject. It is concerned particularly with distinguishing those properties that can be modified during a single lifetime (short-term adaptation) and those properties that cannot, even though they may be highly adaptive (evolutionary adaptation). There is also, it must be said, a school of thought that suggests that many features of organisms are not adaptive at all, either in the short term, or in evolutionary time. For an entertaining introduction to this view (cited more than 1400 times between 1981 and May 2003) read Gould and Lewontin (1979).
Many matters dealt with here are of some complexity, and the author is no doubt guilty of dogmatism in places. I think this is not very important because the purpose of this review is to point up issues concerning the question of adaptation, rather than to give incontrovertible proof that particular points of view are certainly correct.
Section snippets
Woven and lamellar bone
Mammalian bone exists in two usually fairly distinct forms: woven and lamellar. Woven bone is laid down rapidly, its collagen is fine-fibred, and oriented almost randomly (Weiner and Wagner, 1998). It becomes highly mineralised (Pritchard, 1972). Its osteocytes are approximately isodiametric. Lamellar bone is laid down much more slowly, having a more precisely defined structure. It is arranged in lamellae. The collagen and its associated mineral in these lamellae is oriented in the lamellar
Stress concentrations in bone
Most compact bone tissue is riddled with potential stress concentrators, in the form of blood channels, erosion cavities, osteocyte lacunae and canaliculi. A stress concentrator increases the local stress by a factor, SCF, compared with the stress at a distance from the concentrator. (The values given below are for infinitely large homogeneous solids. In bones of finite size the effects will be somewhat smaller.) The extent to which these stress concentrators increase the likelihood of bone
Range of stiffness and toughness in bone
Although most compact bone has roughly the same mechanical properties, there are some really extreme values, ranging from those of some antler bone, which has a Young's modulus of about 5 GPa and is extremely tough (Currey, 1979), to the rostrum of a toothed whale (Mesoplodon densirostris) which has a Young's modulus of about 40 GPa and is extremely brittle (Zioupos et al., 1997). Most of the differences are caused by differences in the amount of mineralisation, although structural anisotropy can
Architecture–material properties synergy
The mechanical properties of whole bones depend both on the material properties of the bone and the architecture of the whole bone. There may be adaptive links between these two features. This is most clearly shown during growth.
Brear et al. (1990) examined a set of five wild polar bear (Ursus maritimus) femurs of known age and weight. The ages ranged from 3 months to 7 years (maturity occurs at about 2 years) and the mass from 9.5 to 400 kg. The bone material was both weaker, having a lower
Secondary remodelling
Internal secondary remodelling is a striking feature of the bone of many ‘higher’ vertebrates, resulting in the production of Haversian bone, in which much of the bone is occupied by secondary osteones (Haversian systems) or interstitial lamellae (the remnants of secondary osteones now cut off from the local blood supply by later secondary remodelling). The reasons for secondary remodelling have been long debated. In the days when bones were seen mainly as temporary stores of calcium and
The hollowness of bones
Most long bones are hollow; this is one of their most striking features. It might seem easy to explain this, because, weight for weight, a hollow cylinder is stiffer and, to a lesser extent, stronger in bending than a solid cylinder. However, the situation is complicated by the fact that the great majority of these hollow long bones are filled with fat. In early life the fat is red and haematopoeitic, but with maturity it is converted to yellow fat, which seems to have little physiological
Conclusions
This survey gives some examples of how bones are adapted to their circumstances. There is a spectrum of immediacy in this adaptation. Some features, such as the amount of mineralisation, are determined in evolutionary time while others, like the positioning of secondary osteons in damaged bone, develop quickly during the life of the animal. Other features are determined both long term and short term. The main purpose of this survey is to remind readers that there are many more adaptations in
Acknowledgements
I thank Steve Cowin for persuading me to write this review and for pointing out that anisotropy had an effect on stress concentrations, and I thank two referees for making important criticisms and suggestions.
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