ARTICLE IN PRESS
Journal of Biomechanics 36 (2003) 1487–1495
The many adaptations of bone
J.D. Currey*
Department of Biology, University of York, P.O. Box 373, York YO10 5YW, UK
Accepted 27 March 2003
Abstract
Studies concerned with the ‘adaptations’ in bones usually deal with modelling taking place during the individual’s lifetime.
However, many adaptations are produced over evolutionary time. This survey samples some adaptations of bone that may occur
over both length scales, and tries to show whether short- or long-term adaptation is important. (a) Woven and lamellar bone. Woven
bone is less mechanically competent than lamellar bone but is frequently found in bones that grow quickly. (b) Stress concentrations
in bone. Bone is full of cavities that potentially may act as stress concentrators. Usually these cavities are oriented to minimise their
stress-concentrating effect. Furthermore, the ‘flow’ of lamellae round the cavities will still further reduce their stress-concentrating
effect, but the elastic anisotropy of bone will, contrarily, tend to enhance it in normal loading situations. (c) Stiffness versus
toughness. The mineral content of bone is the main determinant of differences in mechanical properties. Different bones have
different mineral contents that optimise the mix of stiffness and toughness needed. (d) Synergy of whole bone architecture and
material properties. As bone material properties change during growth the architecture of the whole bone is modified concurrently,
to produce an optimum mechanical behaviour of the whole bone. (e) Secondary remodelling. The formation of secondary osteones in
general weakens bone. Various suggestions that have been put forward to account for secondary remodelling: enabling mineral
homeostasis; removing dead bone; changing the grain of the bone; taking out microcracks. (f) The hollowness of bones. It is shown
how the degree of hollowness is adapted to the life of the animal.
r 2003 Elsevier Science Ltd. All rights reserved.
1. 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
*Tel +44-1904-328589; fax +44-1904-328505.
E-mail address: [email protected] (J.D. Currey).
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.
0021-9290/03/$ - see front matter r 2003 Elsevier Science Ltd. All rights reserved.
doi:10.1016/S0021-9290(03)00124-6
ARTICLE IN PRESS
1488
J.D. Currey / Journal of Biomechanics 36 (2003) 1487–1495
2. 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 plane, and very often has a characteristic
direction, extending over many tens of microns (Boyde,
1980). The collagen is arranged in thicker bundles than
in woven bone. The osteocyte lacunae in lamellar bone
are flattened oblate spheroids. The shorter axis of each
lacuna is oriented parallel to the thickness of the lamella.
The paragraph above is a very simple description of
lamellar bone, and there are still heavily contrasting
views about how, in detail, the tissue is arranged (e.g.
Marotti, 1993; Weiner et al., 1999).
Unfortunately, we know little about the mechanical
properties of woven bone. However, its loose structure
and random orientation makes it almost certain that it is
mechanically inferior to lamellar bone. It is surprising,
therefore, to find woven bone as a characteristic feature
of the mature bone of large dinosaurs, birds and
mammals. This bone is known as fibrolamellar bone
(Francillon-Vieillot et al., 1990). It is found particularly
in large animals, whose bones have to grow quickly. If a
bone has to grow faster than the rate at which lamellar
bone can be laid down, other bone must be laid down
instead. Essentially, an initial scaffolding of woven bone
is laid down quickly to be filled in more leisurely with
lamellar bone. This method of construction results in
alternating layers of woven bone and lamellar bone
tissue wrapped around the whole bone.
Fibrolamellar (often known as ‘plexiform’) bone,
which is primary, seems to be stronger, particularly
when loaded along the grain, than Haversian bone
which in many animals replaces it (Currey, 1959; He#ıt
et al., 1965). However, it is weak and, particularly, very
brittle when it is loaded across the grain (Reilly and
Burstein 1974, 1975). Therefore, when the predominant
direction of loads on fibrolamellar bone changes during
growth, it may well end up being orientated in a highly
disadvantageous direction. In that case, secondary
remodelling may take place, so that the grain of the
bone is altered.
The kind of primary bone laid down depends on the
rate of accretion. Castanet et al. (1996) studied the bones
of the mallard duck Anas platyrhyncos. The humerus
grew fastest, and initially, at 7 weeks of age, had a rate
of accretion of about 25 mm a day; the bone was
completely fibrolamellar. As the rate of accretion
declined the fibrolamellar bone gave way to anatomising
primary osteons, and finally, when the accretion rate
was only about 1 mm a day, the blood vessels were
sparse, and the bone consisted of circumferential
lamellae. The phalanges, on the other hand, which had
a much lower accretion rate right from the start, never
showed any sign of fibrolamellar histology.
We have here an example in which bone is obliged,
because of the rate at which it is laid down, to
incorporate inferior material, but is nevertheless able
to produce a quite superior result by ingenious marrying
together of two histological types. Fibrolamellar structure has been evolved, many times, over evolutionary
time scales, from the simpler bone found in animals with
small bones.
3. 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
breaking is difficult to determine, because the fracture
mechanics properties of bone are themselves not well
understood. Nevertheless, the disposition of these
potential stress concentrators is instructive.
The question of the direction of dangerous stresses in
bones is debatable. It is likely that most fractures of long
bones resulting from accidents are the result of bending.
In this case the main stresses, both tension and
compression, will be along the length of the bone,
though there may, of course, be some torsional loading
as well. Fatigue loading will also produce bending, but
there may be a larger component of compressive
loading. What is certain, however, is that there will
not be large stresses directed radially in the endosteal–
periosteal direction. One might expect, therefore, if the
structure of bone is adapted to reduce the danger of
potential stress concentrators, that the structure will
accord with these directions of loading.
First, the external surfaces of bones are nearly always
rather smooth, without obvious steps or sharp-edged
protuberances or hollows except right at their ends (see
many illustrations in Alexander, 1994). The major blood
vessel traversing the cortex is the nutrient artery, and
this usually has a course that is at a small angle to the
long axis of the bone. SCF for a hollow cylinder loaded
in the x-direction is 1 þ 2 sin y where y is the angle the
cylinder makes with the x-direction. SCF is at worst 3,
therefore, and will be less as it becomes more closely
aligned with the longitudinal direction. Ordinary blood
ARTICLE IN PRESS
J.D. Currey / Journal of Biomechanics 36 (2003) 1487–1495
channels, again, have a mainly longitudinal, though
gently spiralling course in long bones. All such arrangements will minimise the stress-concentrating effect of
these cavities in relation to forces directed mainly along
the length of the bone. Not all blood channels are so
benignly oriented. In particular, Volkmann’s canals run
nearly directly transversely. The blood channels of
fibrolamellar bone are a special case, they are arranged
as a series of two-dimensional anastomosing networks,
flattened in the radial direction. This makes their stressconcentrating effect very small for longitudinal loads,
but large for radial loads.
The lacunae in woven bone are roughly isodiametric
and would have a value of SCF of about 2. The lacunae
of lamellar bone, however, are flattened oblate spheroids
and can have much higher SCFs than a cylinder.
Assuming that the ratio of the major to the minor axis
is 5, typical for such lacunae, they will have a notional
value of SCF of about 1.2 when loaded longitudinally,
but when loaded radially SCF will be more than 7.
Finally, the canaliculi are arranged in all directions, and
SCF will be 3 in the worst direction. So it would seem
that except for the smallest cavities, the canaliculi,
potential stress concentrators in bone are arranged in a
way that minimises their stress-concentrating effect.
However, bone is elastically anisotropic, and its
modulus in the longitudinal axis is greater than in the
directions normal to it (Reilly and Burstein, 1975). This
will have the effect of increasing somewhat the stressconcentrating effect of voids if the load on the bone is
directed primarily along its length (Green and Taylor,
1945; Kaltakci, 1995). Furthermore, stress-concentration factors are worked out assuming that the material is
homogeneous. However, examination of the lamellar
histology in the neighbourhood of stress concentrators
shows that the lamellae ‘flow’ round the concentrators
like the grain in wood round a knot. The forces will tend
to follow the lamellae, and therefore the effect of the
concentrators will be less, possibly much less, than
calculated from theory. Such amelioration does not,
however, apply to secondary osteones, which punch
brutally through pre-existing lamellae, and are not
adapted to their orientation at all.
The arrangement of potentially stress-concentrating
structures in bone is extremely constant through many
bone types, and there is little evidence, except when
lamellar bone as a whole remodels in a new direction,
that their positioning changes during life. This positioning is therefore presumably determined over evolutionary time, and not during ontogeny.
4. Range of stiffness and toughness in bone
Although most compact bone has roughly the same
mechanical properties, there are some really extreme
1489
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 also have some marked effects.
In cases where the overridingly important function of
the bone is clear, the differences in mechanical properties seem appropriate. Antlers are used in fighting, where
impact resistance is of paramount importance. The
antlers have a low mineralisation, and are very strong in
impact. Their Young’s modulus, on the other hand, is
not high, but during the pushing part of a fight it will
not matter if the antlers flex somewhat. The ear bones,
on the other hand, need to be very stiff for acoustical
reasons, and they are highly mineralised, very stiff, weak
and brittle. However, since they are hidden away inside
the skull, the weakness might seem to be immaterial.
Nevertheless, their brittleness may occasionally be
important even inside the head and, for instance, the
mature human periotic bone often has fatigue cracks
(S^rensen et al., 1992). Bone material in ordinary bones
is intermediate in its mineral content, stiffness and
toughness (Currey, 1979).
Younger bone is in general more compliant and
tougher than that of mature animals. However the
stiffness of bone material of a full-term fetus of the Axis
deer Axis axis is as stiff as a human 10-year old. It is
correspondingly less tough (Currey and Pond, 1989).
This is no doubt adaptive because the new-born deer
have to run with the herd very soon after birth, and their
limb bones are quite slender, and would be certain to
buckle if they had the relatively low modulus of a
human new-born. The adults of these deer have a high
mineral content and modulus (28 GPa). This is probably
adaptive for these slender-boned animals, prone to Euler
buckling. For young children, on the other hand,
toughness is more important than stiffness.
There is no evidence that such differences are the
result of adaptations arising because of the loading on
the bones. Human and deer fetuses are in roughly the
same situation, but achieve very different amounts of
mineralisation after nearly the same number of months
in utero. The ear bones are loaded by very low loads
throughout life, and have a very high mineralisation.
Deer’s antlers, on the other hand, are loaded with low
loads until all growth and maturation has ceased, and
yet they have a very low mineralisation. Woo et al.
(1981) found that as a result of exercise, pigs’ bones
became stouter and therefore more resistant to loading,
but the material properties of the bone were unchanged.
It is in the properties over a wide range of
mineralisations that one sees most clearly the inevitable
trade-off between stiffness and toughness. As with
ARTICLE IN PRESS
1490
J.D. Currey / Journal of Biomechanics 36 (2003) 1487–1495
nearly all other materials, it seems to be impossible to
develop bone that is both stiff and tough. Selection has
to act in such a way as to optimise the mechanical
properties of the bone, making it neither too brittle, nor
too compliant. These adaptive differences are almost
certainly determined over evolutionary time, and not
during ontogeny.
5. 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 212 years) and the mass from 9.5 to
400 kg. The bone material was both weaker, having a
lower yield stress, and less stiff, having a lower Young’s
modulus of elasticity, in the younger animals’ bones,
and these differences correlated well with the lower
degree of mineralisation of the younger bones. Does this
mean that the bones themselves were less strong and
stiff? Some simple assumptions were made about the
loading on the bone. The ‘resistance to yielding’ was
loading divided by the strength. The stiffness of the bone
was estimated by the relative shape change, that is the
deflection of the end of the bone divided by the length of
the bone. Bones with the same proportional deflection
would be bent to the same shape, although of course the
absolute deflection of the longer bone would be greater.
The weights of the bears vary by a factor of 40, and the
lengths of the bones by a factor of three, producing
bending moments that vary by a factor of 130, yet the
range of resistances to yielding (a factor of 2.5) and in
the relative shape change (a factor of 3.1) is small. If the
bone material in all the bones had identical mechanical
properties, but the shapes were as they had been
measured, then the resistance to yielding would have
had a range of 5, rather than 2.5, and the shape change
would have a range of 10.3, rather than 3.1. The
implication of these calculations is that the architecture
of the bones is rather precisely adapted to the loads
placed on them and to the mechanical properties of the
bone material.
A study in Californian gulls by Carrier and Leon
(1990) shows similar features to the polar bears, but here
it was possible to study the different behaviour of the leg
bones (used almost from hatching), and the wing bones
(which grew much in diameter only just before the
juvenile started to fly). The bone tissue was initially
weak and compliant in both arms and legs. In the legs
this tissue weakness and compliance was compensated
for by a relatively large cross-sectional shape. The wing
bones grew in length quite steadily. However, they
remained quite slender, and therefore very feeble and
compliant, until just before flying started, when there
was a very large growth spurt in diameter. Bones of both
limbs were functional, therefore, when they were
needed, but the extra diameter needed to compensate
for the feeble tissue was needed initially only in the legs,
but not the wings.
Of course, it is not possible to vary infinitely either the
architecture or the material properties of bones.
Biewener (1982) showed that the strength of the bone
material in bones from animals with a wide range of
body masses was very similar, and it is probable, despite
remarks made in Section 4, that for many long bones in
particular it would not be possible to increase the
strength or Young’s modulus of bone material to any
significant extent. Given this, if the circumstances of two
species are different, it is likely that any major difference
will show itself in the gross morphology rather than in
the bone material itself. For instance, Terranova (1995)
shows that leaping primates that leap more, or land
more heavily, compared to their more sedate relatives
have femora with relatively expanded cross sections.
This increased strength and stiffness will bring with, it
course, a corresponding penalty of increased mass.
These examples show that the material properties of
bones can change in a neat synergy with the architecture
as the function of the bone changes, or is about to
change. Probably, in this case, the material properties
are determined over long, evolutionary, time, while the
architecture of the bones is responding to the strains in
the bone over a short period, although this latter is less
certain.
6. 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 phosphate, it was thought that the
purpose of secondary remodelling was to release the
needed ions into the circulation. However, bone is being
resorbed and deposited at the same time, often almost
contiguously, so any advantage to the body as a whole
must be small. Burton et al. (1989) point out that by the
6 month secondary remodelling is going on intensively
in the human fetus. It seems extraordinarily unlikely
that this remodeling is required by the metabolic needs
ARTICLE IN PRESS
J.D. Currey / Journal of Biomechanics 36 (2003) 1487–1495
of the fetus. If the remodelling is to satisfy the mother’s
metabolic requirements, this would be a bizarre case of
robbing Peter to pay Pauline so that Peter can be repaid.
Various other ideas have been proposed, which are
listed below.
6.1. Mechanical competence
Mechanical studies showed that in both tension and
compression remodelled bone in the middle of long
bones seemed to be weaker than the surrounding
primary fibrolamellar bone (Currey, 1959; He#ıt et al.,
1965). Remodelling seems to have a particularly dire
effect on creep behaviour (Rimnac et al., 1993).
6.2. Cell death and bone age
If bone cells die, the bone tissue around them can be
considered as dead. It is not at all clear in what ways
dead bone is less effective than living bone. However,
there is evidence that secondary osteones may occasionally form where cells have died (Currey, 1960). Bone
that has been in place a long time may become
hypermineralised and therefore brittle. Removing such
bone would be adaptive.
6.3. Changing the grain
Where the imposed forces change in direction in
relation to the grain of the bone, secondary remodelling
can alter the grain of the bone adaptively. This is seen
under large muscle insertions and during fracture repair
(Vasciaveo and Bartoli, 1961). Enlow (1975) shows that
the secondary remodelling seen under muscle insertions
results in muscles having firm attachments to the bone
even when the muscle insertion is migrating during
growth, and also during erosion of the bone surface
when the shape of the bone is being altered. Compact
coarse-cancellous bone, which is bone produced by the
infilling of cancellous bone, is often badly oriented, and
replacing it with well-positioned secondary osteones
might be mechanically advantageous. (Similarly, cancellous bone produced by the erosion of compact bone
will probably not have its grain optimally orientated,
but changing this would involve changing the composition of whole trabeculae, rather than internal remodelling.) However, the usual orientation of secondary
osteones makes it certain that improving the grain of
bone is not their only function. Many of the secondary
osteones developing in long bones do not materially
alter the grain of the bone. They have a mainly
longitudinal, though very gently spiralling, course, and
the blood channels they replace have the same orientation (Cohen and Harris, 1958). Furthermore, in animals
that undergo many generations of remodelling, there
does not seem to be any general change of direction
1491
between earlier and later generations of secondary
osteones.
The work of Riggs et al., (1993a,b) does, however,
suggest that remodelling may change the grain of the bone
in an adaptive manner. Bone in the anterior cortex of
horses’ radii is subjected almost exclusively to tension. It
undergoes little remodelling, and if it does remodel the
resulting secondary osteones tend to have longitudinally
oriented fibres. Unremodelled bone has a predominantly
longitudinal orientation. Bone in the posterior cortex is
subjected mainly to compression, is intensively remodelled,
and the resulting secondary osteons have more predominantly transverse fibres. These striking histological changes
are accompanied by appropriate changes in the mechanical properties. Takano et al., (1999) observed changes in
the mechanical anisotropy of the collagen in dog’s radii
that were correlated with the changes in strain induced by
osteotomy. Although they did not apparently examine the
histology of the bone, and found the structural anisotropy
to be too variable to show significant changes, it is not
really possible for the mechanical anisotropy to have
changed except by secondary remodelling.
6.4. Taking out microcracks
An obvious possible function of remodelling is to
repair damage in the bone. Burr et al. (1985) showed
that if dogs’ bones were loaded in fatigue, they had a
large number of microcracks, and these microcracks
were associated with remodelling resorption cavities
more often than could be accounted for by chance. The
obvious explanation for this is that the resorption
cavities are there because secondary remodelling is
getting rid of the microcracks. However, it could be
that the resorption cavities produce stress concentrations and that microcracks develop in these regions.
However, by clever experimentation Mori and Burr
(1993) showed that the obvious explanation was also
much the more likely one. Using the time course of the
development of secondary remodelling they showed that
immediately after being damaged, erosion cavities in
bone were less numerous and were much less commonly
associated with erosion cavities than when a week had
been allowed to pass after the damage was produced.
So, resorption came after microcracking, and was
spatially related to it. Finally, an experiment by
Bentolila et al. (1997) showed that fierce fatigue loading
of rats’ bone, producing many microcracks, induced
internal remodelling in the microcracked regions. In this
case there can be no doubt that the remodelling was a
response to damage.
6.5. Other considerations
The distribution of remodelling in different species of
vertebrates is instructive. In general, in the ‘lower’
ARTICLE IN PRESS
1492
J.D. Currey / Journal of Biomechanics 36 (2003) 1487–1495
vertebrates, that is, all vertebrates except the mammals
and birds, there is rather little secondary remodelling.
The dinosaurs and some of the larger mammal-like
reptiles do, however, show many secondary osteones. If
one were to hold to the idea of secondary osteones
functioning by eliminating microcracks, one could
explain this distribution of secondary remodelling either
by supposing that reptiles and amphibians do not suffer
fatigue cracks or that they are unable, for some
physiological reason, to remodel. It is indeed possible
that reptiles suffer less microcracking in their bones
because, being generally sluggish, the penalties to them
for having overdesigned bones, with great safety factors,
would be less than for active mammals or birds.
In the mammals and birds extensive internal remodelling seems to go with size of bone rather than anything
else. Biewener (1983) showed that there is a reasonable
consistency in the calculated greatest strains produced
by locomotion in bones of very different sizes. So, it
would seem that remodelling is a function of bone size,
as well as strain. Small birds’ bones have very narrow
cortices, and remodelling is almost absent. Ostriches, on
the other hand, have extensive Haversian bone. In
mammals, the larger primates and carnivores, perissodactyls and artiodactyls show much remodelling, the
smaller mammals rather little, even though some are
quite long-lived. The distribution of remodelling in the
larger artiodactyls is interesting because one finds in a
cross section of say, the femur, that most of the bone
may be still primary fibrolamellar bone, with occasional
isolated secondary osteones, but that in one part of the
section the bone has been completely remodelled.
Usually, this remodelling is under a place where large
muscles insert. This general distribution of remodelling
in birds and mammals does not correspond well with
what one feels is likely to be the distribution of more or
less highly stressed bone.
Finally, in nearly all tetrapods that show remodelling,
the remodelling that does take place seems usually to be
more intense toward the marrow cavity than toward the
subperiosteal part of the bone (Atkinson and Woodhead, 1973; Bouvier and Hylander, 1981. Bouvier and
Hylander gave monkeys hard or soft diets and observed
more secondary osteones in the mandibles of the harddiet group. The remodelling was sparse in the subperiosteal region, however. In commenting on this they
suggest that, because of the way the mandible grows, the
subperiosteal bone was younger, and therefore had had
less time to develop fatigue cracks and to be remodelled.
In summary, there are several explanations for the
phenomenon of secondary remodelling, and there is
some evidence for the validity of some of them. Perhaps
the three most compelling are those that involve taking
out microcracks, changing the grain of the bone, and
renewing bone that, simply because of its age, may be
hypermineralised and weaker (though it may also be
developing microcracks). Nevertheless, the way in which
remodelling seems to be programmed, particularly on
the endosteal side of the cortex of long bones, does make
it seem that there is another factor of which we are
ignorant.
Although the ability to remodel and the mechanism
that determined how and when it occurs are no doubt
determined over evolutionary time scales, most suggestions as to the function of remodelling require that it
occur in response to factors acting during the animals’
lifetimes.
7. 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
function. The fat seems not to be used except in the final
stages of starvation, and so usually must be acting as
useless packing material. Certainly, there is no good
evidence that it has any significant mechanical function
(Arramon and Cowin, 1997). As the bone is made ever
thinner-walled and stouter, the weight of the whole bone
will at first decrease, but will then start to increase, as
the weight of the fat becomes greater than the saving in
weight of the bone. Currey and Alexander (1985)
showed that, for various kinds of loading, the maximum
saving in mass was not very large (at most about 15%)
though certainly worth striving for. They also showed
that the hollowness of the bones was such that they were
near the optimum for weight saving
Some birds and many pterodactyls (Gower, 2001),
however, have managed to empty some of their long
bones of fat, replacing it with gas, so that they can
achieve a very thin-walled architecture. Some pterodactyl’s bones are remarkable, having a diameter to wall
thickness ratio of 25:1. This is a ratio which, given the
Young’s modulus of bone, would imply that the mode
of failure is likely to become local buckling. Local
buckling is very sensitive to local pressures, and this fact
in turn implies that these pterodactyls must have had
rather sedate lives. Surprisingly, these very thin-walled
cylinders seem rarely to have internal cross-struts, which
would have sharply reduced their tendency to buckle.
Cross-struts are found, however, in one exceptionally
thin-walled pterodactyl humerus, whose diameter to
wall-thickness was 30:1 (Wellnhofer, 1985).
It is interesting that the mammals seem not to have
evolved air-filled bones which must, in some circum-
ARTICLE IN PRESS
J.D. Currey / Journal of Biomechanics 36 (2003) 1487–1495
stances, be adaptive. It is a difficult anatomical feat,
because the air sacs spread from the lungs, and enter the
bones through little foramina. Perhaps this is one
example of an evolutionary adaptation which was
achieved by only two of the three free-flying vertebrate
groups (bats do not have air-filled bones) because of the
sheer difficulty of doing so.
At the other end of the scale are animals that have
solid, or virtually solid bones. These are the alligators
and the manatees (sea cows). This again seems adaptive,
because these water-living animals have lungs, and so
would tend to be positively buoyant in water. Having
thick-walled bones is a way of achieving neutral
buoyancy, while getting rid of more or less valueless
fat. Domning and de Buffre! nil (1991) have suggested a
slightly more subtle reason. They point out that the total
skeletal mass in dugongs as a proportion of the total
body mass is not greatly different from that of land
mammals. Furthermore, not all the bones of the
manatee and the dugong are thickened and solid, this
phenomenon being restricted to the bones near the
middle of the length of the body. They suggest that the
main function of the solidity of these bones is to help
balance, concentrating the weight of the animal over the
lungs, so that as the lungs expand and contract they do
not produce a change in the trim of the animal, causing
it to go nose up or nose down, which would happen if,
say, the skull were heavy and dense. The lungs
themselves are greatly elongated, and have a spatial
arrangement that tends to confirm the suggestion of
Domning and de Buffre! nil.
Whales do not have very dense bones. Wall (1983)
attributes this fact, reasonably enough, to the great
depth of dive of most whales. At depth the lungs are
collapsed and barely contribute to buoyancy. As a
result, in whales, selection pressure to reduce density
and mass will be present, as it is land mammals. For
some unknown reason whales’ bones do not divide
neatly into compact bone and marrow, so it is not
possible to calculate useful ratios of diameter to
thickness.
Oxnard (1993) has produced examples of land
animals with solid long bones. The extinct ground
sloth and some very large extinct marsupials, Zygomaturus and Palorchestes, shared two characteristics, they
were very slow moving, and they had solid bones. He
suggests that these bones may have been optimally
adapted for withstanding axial compression. If they
were loaded only in compression, that would indeed be
optimal, because there would be no marrow fat to
produce. However, it is difficult to believe that these
bones were not frequently loaded in bending, and that
bending would not be the most dangerous mode of
loading.
These examples of different hollowness of long bones
show that in general the variation seems to be adaptive.
1493
I have assumed throughout the Panglossian view that
‘‘all is for the best in this the best of all possible worlds’’
but of course things do not always work out to be
exactly as theory would require, particularly if one takes
only mechanical properties onto account. For example,
in the semi-aquatic Nile monitors Varanus niloticus both
males and females start off with about the same values
for R=t in the femur, but in the females the endosteal
cavity gets relatively larger as they undergo more egglaying cycles (de Buffre! nil and Francillon-Vieillot,
2001). The females lose bone while producing the eggs,
and do not fully regain it before the next eggs develop.
As a result the bones become relatively thin-walled. This
is probably not mechanically the optimum state of
affairs, but is probably the best that can be done from
the point of view of the female monitors. So, it is always
important to consider, as best one can, nonmechanical
factors that may have an effect on the form of bones.
Furthermore, there are a few anomalies that do not
seem readily explicable either in mechanical or more
‘biological’ terms. Such adaptations must to some extent
be determined during the life course of the animals.
However, the subtlety of the algorithms that would
allow ab initio the optimum solution according to
whether the animals had fat or not, or whether they were
aquatic or not, would seem tremendous, and there must
presumably be a great deal of evolutionary determination. (It must be remembered that the algorithm natural
selection works on is simple: ‘If it breaks, throw it out; if
it works, keep it, even if it is slightly different from last
year’s model.’).
8. 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 bone than those produced during a single
lifetime.
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.
ARTICLE IN PRESS
1494
J.D. Currey / Journal of Biomechanics 36 (2003) 1487–1495
References
Alexander, R.McN., 1994. Bones: The Unity of Form and Function.
Weidenfeld and Nicholson, London.
Arramon, Y.P., Cowin, S.C., 1997. Hydraulic strengthening of
cancellous bone. Forma 12, 209–221.
Atkinson, P.J., Woodhead, C., 1973. The development of osteoporosis.
A hypothesis based on a study of human bone structure. Clinical
Orthopaedics and Related Research 90, 217–228.
Bentolila, V., Hillam, R.A., Skerry, T.M., Boyce, T.M., Fyrhie, D.P.,
Schaffler, M.B., 1997. Activation of intracortical remodeling in
adult rat long bones by fatigue loading. 43rd Meeting, Orthopaedic
Research Society, San Francisco, p. 578.
Biewener, A.A., 1982. Bone strength in small mammals and bipedal
birds: do safety factors change with body size? Journal of
Experimental Biology 98, 289–301.
Biewener, A.A., 1983. Allometry of quadrupedal locomotion: the
scaling of duty factor, bone curvature and limb orientation to body
size. Journal of Experimental Biology 105, 147–171.
Bouvier, M., Hylander, W.L., 1981. Effect of bone strain on cortical
bone structure in macaques (Macaca mulatta). Journal of
Morphology 167, 1–12.
Boyde, A., 1980. Electron microscopy of the mineralizing
front. Metabolic Bone Disease and Related Research 2 (Suppl),
69–78.
Brear, K., Currey, J.D., Pond, C.M., 1990. Ontogenetic changes in the
mechanical properties of the femur of the polar bear Ursus
maritimus. Journal of Zoology London 222, 49–58.
Burr, D.B., Martin, R.B., Schaffler, M.B., Radin, E.L., 1985. Bone
remodeling in response to in vivo fatigue microdamage. Journal of
Biomechanics 18, 189–200.
Burton, P., Nyssen-Behets, C., Dhem, A., 1989. Haversian bone
remodeling in the human fetus. Acta Anatomica 135, 171–175.
Carrier, D., Leon, L.R., 1990. Skeletal growth and function in the
California gull (Larus californicus). Journal of Zoology, London
222, 375–389.
Castanet, J., Grandin, A., Abourachid, A., De Riql"es, A., 1996.
Expression de la dynamique de croissance dans la structure
de l’os p!eriostique chez Anas platyrhyncos. Comptes rendus
de l’Academie de Sciences Paris. Sciences de la vie 319,
301–308.
Cohen, J., Harris, W.H., 1958. The three-dimensional anatomy of
Haversian systems. Journal of Bone and Joint Surgery 40-A,
419–434.
Currey, J.D., 1959. Differences in the tensile strength of bone of
different histological types. Journal of Anatomy 93, 87–95.
Currey, J.D., 1960. Differences in the blood-supply of bone of different
histological types. Quarterly Journal of Microscopical Science 101,
351–370.
Currey, J.D., 1979. Mechanical properties of bone with greatly
differing functions. Journal of Biomechanics 12, 313–319.
Currey, J.D., Alexander, R.McN., 1985. The thickness of the walls of
tubular bones. Journal of Zoology, London 206A, 453–468.
Currey, J.D., Pond, C.M., 1989. Mechanical properties of very young
bone in the axis deer (axis axis) and humans. Journal of Zoology,
London 218, 59–67.
de Buffr!enil, V., Francillon-Vieillot, H., 2001. Ontogenetic changes in
bone compactness in male and female Nile monitors (Varanus
niloticus). Journal of Zoology, London 254, 539–546.
Domning, D.P., de Buffr!enil, V., 1991. Hydrostasis in the Sirenia:
quantitative data and functional interpretations. Marine Mammal
Science 7, 331–368.
Enlow, D.H., 1975. A Handbook of Facial Growth. W. B. Saunders,
Philadelphia.
Francillon-Vieillot, H., de Buffr!enil, V., Castanet, J., G!eraudie, J.,
Meunier, F.J., Sire, J.Y., Zylberberg, L., de Ricql"es, A., 1990.
Microstructure and mineralization of vertebrate skeletal tissues. In:
Carter, J.G. (Ed.), Skeletal Biomineralization: Patterns, Processes
and Evolutionary Trends, Vol. 1. Van Nostrand Reinhold, New
York, pp. 471–530.
Gould, S.J., Lewontin, R.C., 1979. The spandrels of San Marco and
the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal society of London 205B,
581–598.
Gower, D.J., 2001. Possible postcranial pneumaticity in the last
common ancestor of birds and crocodilians: evidence from
Erythrosuchus and other mesozoic archosaurs. Naturwissenschaften 88, 119–122.
Green, A.E., Taylor, G.I., 1945. Stress systems in aeolotropic plates,
III. Proceedings of the Royal Society 184A, 181–195.
#
He#ıt, J., Kufera,
P., V!avra, M., Volen!ık, K., 1965. Comparison of the
mechanical properties of both the primary and Haversian bone
tissue. Acta Anatomica 61, 412–423.
Kaltakci, M.Y., 1995. Stress concentrations and failure criteria in
anisotropic plates with circular holes subjected to tension or
compression. Computers and Structures 61, 67–78.
Marotti, G., 1993. A new theory of bone lamellation. Calcified Tissue
International 53 (Suppl. 1), S47–S55.
Mori, S., Burr, D.B., 1993. Increased intracortical remodeling
following fatigue damage. Bone 114, 103–109.
Oxnard, C.E., 1993. Bone and bones, architecture and stress,
fossils and osteoporosis. Journal of Biomechanics 26 (Suppl. 1),
63–79.
Pritchard, J.J., 1972. General histology of bone. In: Bourne, G.H.
(Ed.), The Biochemistry and Physiology of Bone, 2nd Edition.
Academic Press, New York, pp. 1–20.
Reilly, D.T., Burstein, A.H., 1974. The mechanical properties of
cortical bone. Journal of Bone and Joint Surgery 56-A,
1001–1022.
Reilly, D.T., Burstein, A.H., 1975. The elastic and ultimate properties of compact bone tissue. Journal of Biomechanics 8,
393–405.
Riggs, C.M., Lanyon, L.E., Boyde, A., 1993a. Functional associations
between collagen fibre orientation and locomotor strain direction
in cortical bone of the equine radius. Anatomy and Embryology
187, 231–238.
Riggs, C.M., Vaughan, L.C., Evans, G.P., Lanyon, L.E., Boyde, A.,
1993b. Mechanical implications of collagen fibre orientation in
cortical bone of the equine radius. Anatomy and Embryology 187,
239–248.
Rimnac, C.M., Petko, A.A., Santner, T.J., Wright, T.M., 1993. The
effect of temperature, stress and microstructure on the
creep of compact bovine bone. Journal of Biomechanics 26,
219–228.
S^rensen, M.S., Bretlau, P., J^rgensen, M.B., 1992. Fatigue microdamage in perilabyrinthine bone. Acta Otolaryngologica (Stockholm) 496, 20–27.
Takano, Y., Turner, C.H., Owan, I., Martin, R.B., Lau, S.T.,
Forwood, M.R., Burr, D.B., 1999. Elastic anisotropy and
collagen orientation of osteonal bone are dependent on the
mechanical strain distribution. Journal of Orthopaedic Research
17, 59–66.
Terranova, C.J., 1995. Leaping behaviors and the functional morphology of strepsirhine primate long bones. Folia Primatologica 65,
181–201.
Vasciaveo, F., Bartoli, E., 1961. Vascular channels and resorption
cavities in the long bone cortex. Bovine Bone. Acta Anatomica 47,
1–33.
Wall, W.P., 1983. The correlation between high limb-bone density and
aquatic habits in recent mammals. Journal of Paleontology 57,
197–207.
ARTICLE IN PRESS
J.D. Currey / Journal of Biomechanics 36 (2003) 1487–1495
Weiner, S., Traub, W., Wagner, H.D., 1999. Lamellar bone: ´
structurefunction relations. Journal of Structural Biology 12,
241–255.
Weiner, S., Wagner, H.D., 1998. The material bone: structure–mechanical
function relations. Annual Review of Materials Science 28, 271–298.
Wellnhofer, P., 1985. Neue pterosaurier aus der Sanatana-formation
(apt) der Chapada do Araripe, Brasilien. Palaeontographica (A)
187, 105–182.
1495
Woo, S.L-Y., Kuei, S.C., Amiel, D., Gomez, M.A., Hayes, W.C.,
White, F.C., Akeson, W.H., 1981. The effect of prolonged physical
training on the properties of long bone: a study of Wolff’s law.
Journal of Bone and Joint Surgery 63-A, 780–787.
Zioupos, P., Currey, J.D., Casinos, A., Buffr!enil, V., De. 1997.
Mechanical properties of the rostrum of the whale Mesoplodon
densirostris, a remarkably dense bony tissue. Journal of Zoology,
London 241, 725–737.