Annals of Botany 86: 913±920, 2000
doi:10.1006/anbo.2000.1261, available online at http://www.idealibrary.com on
B OTA N I CA L B R I E F I N G
Mechanical Defences to Herbivory
P E T E R W. L U CA S *{, I A N M . T U R N E R {, NAT H A N I E L J . D O M I N Y {
and N AY U TA YA M A S H I TA{
{Department of Anatomy, University of Hong Kong, Li Shu Fan Building, 5 Sassoon Road, Hong Kong S.A.R.,
P.R. China and {Singapore Botanic Gardens, National Parks Board, 1 Cluny Road, Singapore,
Republic of Singapore 259569
Received: 27 March 2000 Returned for revision: 5 June 2000 Accepted: 11 July 2000
The two major mechanical defences of plants are toughness and hardness. These have di€erent material causes and
ecological functions. In any non-metal, high toughness is achieved by composite construction (i.e. by an organized
mixture of components). The primary source of toughening in plants is the composite cell wall (cellulosic micro®brils
set in a hemicellulose and, sometimes, lignin matrix), with a toughness of 3.45 kJ m ÿ2, which is ten-times the
probable toughness of its individual components if they could be isolated. The toughness of most plant tissues is
roughly proportional to the volume fraction of tissue occupied by cell wall (Vc) and, compared to animal tissues and
non-biological composites, is very low. High toughness in plant cells is not produced by the walls themselves, but by
their plastic intracellular collapse. This is a truly cellular toughening mechanism, one of the most potent ever
discovered by materials scientists, depending on an elongate cell shape with micro®brils directed uniformly at a small
angle to the cellular axis. Only `woody' cells, tracheids and ®bres, have this framework and only in the S2 layer of
their secondary wall. Despite this non-optimum con®guration, toughness is elevated by this mechanism ten-times
above that due to cell wall resistance alone. The e€ectiveness of toughness in preventing herbivory is indisputable, but
largely indirect due to confusion over a false equivalence between nutritional `®bre content' and toughness. In
contrast, generalized hardness requires high density. If hardness is due to high Vc , this con¯icts with `woody'
toughness because there is then no lumen for cell walls to collapse into. Thus, dense seed shells may be brittle (i.e. low
toughness) even if built from ®bres. However, solid cell wall is not very hard. Instead, high hardness in plants is
associated with amorphous silica and is always localized. The ecacy of hardness is more dicult to evaluate than
# 2000 Annals of Botany Company
toughness because some animals specialize in coping with it.
Key words: Review, hardness, toughness, mechanical defence, herbivory, cell wall, plastic buckling, silica.
I N T RO D U C T I O N
Mechanical defences are required by a plant in order to
withstand environmental pressures, such as damage by
wind, and to fend o€ herbivores. This article focuses purely
on herbivory. Defences against this can be divided into two
general groups: (1) If cracks can be prevented from starting
in any given plant part, then nothing can be ingested. The
characteristic of this class of defence is hardness. Examples
are seed shells, spines, thorns and sti€ hairs. While seed
shells may achieve this by the density of the cell wall, spines,
thorns and sti€ hairs often include amorphous silica or
inorganic crystals. Coupled usually with sharpness, this
group of defences acts, at one extreme, to deter a herbivore
from contact with the plant or, at the other, by wearing the
contact parts of any animal that attempts to feed. Thus, for
example, a mammal may feed on a plant with such
defencesÐbut not for long without incurring costs due to
dental wear. (2) Cracks may be allowed to begin in the plant
part but crack growth is resisted so as to avoid the tissue
being detached by the wind or a herbivore. A general
characteristic of such defences is high toughness.
* For correspondence. Fax (852) 28170857, e-mail pwlucas@hkucc.
hku.hk
0305-7364/00/110913+08 $35.00/00
Though mechanical defences have frequently been
invoked as important for plants, the underlying mechanisms that produce this have received little attention,
particularly in comparison to chemical defences. Better
understanding and quanti®cation is bound to result in a
more accurate assessment of their importance. This paper
attempts to outline mechanisms by which mechanical
defences obtain their e€ectiveness and also brie¯y reviews
the evidence in preventing losses to herbivores.
SOME BRIEF DEFINITIONS
The action of a force on a plant part produces a displacement (which is the movement of any given point within the
structure acted on, measured in the direction of that force).
To predict the intensity of this disturbance to the shape and
integrity of the structure, both force and displacement have
to be normalized to its size. The quantities of stress and
strain achieve this. Stress is the concentration of a force and
is obtained by dividing a force by the area over which it
acts. Strain is the ratio of the displacement to the size of the
structure, where size is the linear dimension of the structure
in the direction of the force. At small strains in plant tissues,
the response is largely elastic and stress and strain are
# 2000 Annals of Botany Company
914
Lucas et al.ÐMechanical Defences to Herbivory
usually proportional to each other. Their ratio is called
Young's modulus. Since strains are dimensionless, Young's
modulus has the dimensions of stress. The Pascal is an
engineering unit meaning 1 Newton per square metre. It is a
very small unit and we therefore use MegaPascals
(1 MPa ˆ 106 Pa) or GigaPascals (1 GPa ˆ 109 Pa) for
describing it. In natural and arti®cial materials, Young's
moduli range between 10 ÿ3 MPa for gels to 102 GPa for
ceramics.
A critical transition in the loading of a structure is either
a permanent change of shape or the initiation of a crack.
The failure of a structure by a crack or cracks takes place at
a characteristic stress. Brittle fracture is the initiation of a
crack in the structure at a stress that is usually called the
fracture strength. Fracture strengths are actually sizedependent: larger structures of a given tissue or material
fail at lower stresses. The yield strength of a material is a
true material propertyÐthe stress at which permanent
deformation starts in a tissue.
Fracture strength is not a `true' material property in that
it is size-dependent. All specimens of materials are somehow ¯awed, the size of the ¯aws depending on the size of
specimen. The growth of these ¯aws is controlled by a
property called toughness. Toughness is the ability to resist
crack growth and is de®ned as the energy consumed in
growing a crack of given area. Its units are Joules per square
metre (J m ÿ2) or a unit 1000-times larger (kJ m ÿ2). High
toughness does not mean that a solid is strong, or vice versa,
and, in general, high toughness is incompatible with high
strength. As a concept developed only in the twentieth
century, toughness was relatively unknown to biologists
until recently. Landmarks introducing it to a wide audience
were books by Gordon (1968, 1978). The range of toughness in materials lies between 1 J m ÿ2 ( for gels) and
100 kJ m ÿ2 ( for metals) though the extremes are not well
documented. In biological structures, Laminaria digitata
fronds have a toughness 51 J m ÿ2 along the laminae
(Vincent and Gravell, 1986), while mammalian skin
(Purslow, 1983), horse hoof (Bertram and Gosline, 1986),
human ®ngernail (Pereira et al., 1997) and wood across the
grain (Jeronimidis, 1980a) can have a toughness
415 kJ m ÿ2.
Hardness is a term that can refer to elastic or plastic
resistance. It is not actually a property but a traditional
mechanical test (of continued importance, particularly due
to its non-destructive characterÐLawn, 1993) whereby a
pointed object, usually a ball, inverted pyramid or cone is
pushed into a structure. The force divided by the apparent
area of penetration (the area measured in the plane of the
indented surface) is termed the hardness. If the indentation
is permanent (which it almost always is), then hardness
must be related to yield strength. It turns out, for an
indentation of sucient size, that materials which do not
collapse into themselves (densify) much when compressed,
have a hardness that is approximately three-times their yield
strength (Tabor, 1951). Some plant tissues, however,
collapse almost totally into themselves: their hardness is
about the same as their yield strength (Wilsea et al., 1975).
Hardness has the units of stress and is usually pre®xed by a
name that refers to indenter geometry. Only values for
Vicker's microhardness, based on a small pyramidal
diamond, will be quoted here (N.B. in MPa, which is the
proper SI unit). We do not advise smaller measurements
(i.e. indentations 51 mm diagonal length, measured in the
plane of the surface) because, for reasons not yet clear, the
hardness of objects measured by such nanoindentations can
be elevated above the plateau level seen in micro- and
macro-tests (a macro-test produces indentations in the
millimetre range). A ceramic like the enamel of human teeth
has a hardness around 3500 MPa (Waters, 1980), which is
greater than that of mild steel, while the densest seed shell
has a hardness of about 300 MPa (Lucas, 1991).
The above is simple and brief. To learn more about the
basics of materials science, we suggest two volumes by
Ashby and Jones (1980, 1986). Fracture mechanics is a
specialization of engineering and materials science dealing
with toughness. Its theory is still developing and the reader
must expect considerable disagreements between di€erent
authors on both methods of analysis and experiment. Over
biological solids, most of these disagreements centre on the
acceptability of assumptions about their behaviour. The
only text on fracture mechanics (toughness) that refers to
biomaterials is that of Atkins and Mai (1985). Their point
of view is adopted here. Gibson and Ashby (1997) have
expounded a general theory of cellular solids. Vincent
(1990, 1992) describes most of the standard methods of
measurement. It is worth noting (1) that most measurements of toughness necessitate equipment that controls
displacement (thus ruling out experiments with dead
weights); and (2), that only the specimen should deform
during a test, not the testing equipment. When these two
requirements are put together, the result is the large
universal testing machines seen in mechanical engineering
laboratories. With some limitations, particularly over
forces, these machines can, however, be downsized into
portable designs (Darvell et al., 1996).
TYPES OF DEFENCE
We can formalize defences further and propose two basic
strategies that a plant could employ to deter herbivores
from eating its tissues: (a) making a structural component
fail at such a large displacement that it limits the degree of
detachment that a herbivore could achieve in a given time.
This is a ploy that deters feeding by slowing an animal
down. Following Ashby (1999), we will refer to this as
displacement-limited defence. The most important feature
of this type of defence is either the toughness of the plant
part alone if it is very thin or the ratio of its toughness to
Young's modulus if it is fat. (b) Making a structural
component break at a force higher than a herbivore could
achieve without its own structure failing. We have to re®ne
this statement because any actual loading of an object
involves a contact area that dissipates the load. The stress at
any location within the object de®nes this dissipation.
Stresses in a solid object have to exceed a critical value or
nothing will happen. Following Ashby (1999), we will refer
to this as stress-limited defence. Plant defences that depend
on preventing cracks starting are largely of this
Lucas et al.ÐMechanical Defences to Herbivory
stress-limited kind and depend for their e€ectiveness on a
high yield stress, i.e. high hardness.
In order to grasp the general di€erence between these as
potential defences, we o€er an illustrative example. Consider approaching a small tree and bending a horizontal
branch downwards, grasping it with your arm, with the
intention of cracking and detaching it purely with this
downward motion. Pressing down on the branch, there are
two possible limits which could be reached and which could
prevent you starting a crack in it. You could bend it
through 90 degrees right against the trunk without success.
This is a displacement-limited situation: there was sucient
stress but you ran out of displacement. This can form the
basis of a plant defence. The toughness of the branch is very
important in the design of such a defence, but a quanti®ed
analysis shows it to depend on the square root of the ratio
of its toughness to its Young's modulus (Ashby, 1999).
Alternatively, the branch may resist with little de¯ection,
not cracking because you cannot provide sucient force.
This is stress-limitation: there was sucient displacement
available but you lacked the force to generate the stress. A
high hardness is usually a sucient mechanism for such a
defence. This stress-limited defence is probably easier to
overcome than a displacement-limited defence, which is far
more important overall.
Though we will largely concentrate on factors that
produce toughness and hardness in plant tissues, we will
®rst describe what these properties mean more basically in
terms of plant structure.
Displacement-limited defence
The basis for the toughness of plant tissues is the cell
wall. Cell wall, known to nutritionists as ®bre, is a
mechanical compositeÐan organized mixture of two or
more components. The Young's modulus and yield strength
of a composite must always lie within bounds imposed by
the properties of the components. The composite cannot be
sti€er or stronger than the sti€est and strongest of its
components (Harris, 1980; Ashby, 1993). As with other
materials, the presence of ¯aws reduces their strength but
their success lies in a structural organization that promotes
toughness because there can be synergy between components, elevating toughness far above that of the components in isolation. This toughness prevents small ¯aws
from propagating through the composite. Cell walls are an
example. Cellulose is either a crystalline solid or a liquid
crystal (Vincent, 1999) with a theoretical toughness
510 J m ÿ2 (Hiller et al., 1996). We are less clear about
hemicelluloses, but lignin, if it could ever be extracted, is a
highly cross-linked polymer, rather like an adhesive, and
thus unlikely to have a toughness 4300 J m ÿ2. A composite has a ratio of toughness to Young's modulus that is
several decades higher than that of its separated components and has a suitable design for displacement-limited
defences.
We will say no more about Young's modulus and
concentrate on toughness. What is the toughness of the
intact cell wall? There are two ways to get an estimate. The
best method is indirect, measuring the toughness of
915
relatively homogeneous tissues with di€erent volume
fractions of cell wall, Vc (limits of 0.0±1.0), and then
extrapolating the trend line to a ®ctive tissue with solid cell
wall (i.e. Vc ˆ 1.0). Cutting tests can be used for this
(Fig. 1). Measuring the toughness of a plant part with a
scissors cutting test is relatively straightforward: ®nd the
work needed to fracture the tissue being sure to subtract
work done against friction (Vincent, 1992). A tissue cannot
be characterized by the mean of a few tests because,
whenever a cell is fractured, there is some energy expended
in plastically displacing the wall into the centre of the cell,
an e€ect that requires separate quanti®cation. Also, work is
done within the cell wall both in elastic (recoverable)
deformation at the crack surfaces and in permanent damage
around the crack tip in what is termed the plastic zone. It
turns out, in similar tests on other materials, that the
amount of plastic work is independent of test specimen
thickness when this is greater than the size of the plastic
zone, but as thickness is reduced, is proportional to it.
Thus, the gradient of a plot of toughness vs. specimen
thickness re¯ects the work done in plastic distortion
(Fig. 1B). Toughness should plateau when specimen thickness is of the order of the diameter of the plastic zone. A
true plateau is not usually found but signi®cant deviation
from linearity usually begins between 0.5±1.0 mm. A
regression line for tests on thinner specimens allows an
extrapolation to zero thickness, when no cellular space
could exist, and removes both plastic e€ects. From this
analysis, an estimate for the elastic toughness of the wall of
82 plant tissues and plant-based materials (Lucas et al.,
1995, 1997) is 3.45 kJ m ÿ2 (Fig. 1D). There appears to be
little di€erence between tissues with di€erent wall structures.
A direct test is also possible on cells large enough to be
contacted individually by a microprobe. Hiller et al. (1996)
used such a microprobe on the primary cell wall of the
parenchyma of potato tubers and measured an average
toughness for the cell wall of 9.55 kJ m ÿ2, of which these
authors estimate one-third, or 3.18 kJ m ÿ2, of this as being
due to elastic mechanisms. This is in very good agreement
with the indirect estimate of 3.45 kJ m ÿ2 above. The actual
elastic mechanisms by which this toughness is achieved are
unclear. Some pull-out of cellulosic micro®brils from the
surrounding hemicellulose-lignin matrix is probable, a
mechanism which elevates toughness by frictional e€ects
in arti®cial composites (Harris, 1980). The friction of pullout o€ers only a toughness increment of a few hundred
J m ÿ2, but as these micro®brils pull out, they seem to
bridge over the crack surfaces restraining crack opening
(Fig. 1C). This is likely to make a larger contribution
(Lawn, 1993).
Impressive as 3.18±3.45 kJ m ÿ2 may appear to be, the
cell wall is not really a model composite. Its toughness
should be compared to the 50 kJ m ÿ2 or more typical of
carbon, boron or glass ®bre reinforced composites (Atkins
and Mai, 1985). There is, however, a second toughening
mechanism in woody tissues. Woody tissues have elongated
support cells called ®bres (in angiosperms) or tracheids (in
both angiosperms and gymnosperms). These cells have
cellulose micro®brils in the S2 layer of their secondary cell
916
Lucas et al.ÐMechanical Defences to Herbivory
A
Toughness (kJm–2)
15
100 µm
10
5
0
0
1
2
Section thickness (mm)
40
D
30
Sitka spruce
20
Teak
10
Balsa
Plastic work (MJm–3)
Toughness (kJm–2)
40
C
B
3
E
30
10 µm
1º cell wall
pod/seed coat
woody gall
tropical wood
temperate wood
climber
seed shell
20
10
0
0
0
0.25
0.5
0.75
1.0
Cell wall volume fraction, Vc
0
0.25
0.5
0.75
1.0
Cell wall volume fraction, Vc
F I G . 1. Scissors cutting tests allow the partition of toughness contributions in plant tissue between the cell wall and its potential plastic collapse. A
shows a free-running wavy crack passing straight across the grain in front of the scissor blades (optical section by laser-scanning confocal
microscopy). Cutting tests are required to constrain cracks to paths that they would otherwise avoid. B, Multiple tests on one tissue (a light wood)
varying its section thickness. A regression line for all points 50.5 mm produces a slope and a y-intercept, these data being used in the other graphs
shown. C, Scanning electron micrograph of the crack tip ahead of the blades showing remnants of bridging ligaments. These remnants have been
plastically stretched while most of the wall appears to have fractured in a brittle manner. D shows the y-intercepts for 82 plant tissues or plantbased materials (range of Vc from 0.003±0.96), plotted against Vc (measured by `relative density' for woods and seed shells and microscopically for
most other tissuesÐGibson and Ashby, 1988). There is no sign of non-linearity and the intercept is not signi®cantly di€erent from zero.
Toughness of solid cell wall (Vc ˆ 1.0) is predicted as 3.45 kJ m ÿ2, apparently independent of wall structure and, therefore, equivalent to `®bre
content'. Circles are means of data for three woods from more complex fracture tests, not including scissors or cutting (Jeronimidis, 1980a).
Clearly, the properties of the cell wall cannot explain these toughness values. E shows slopes plotted against Vc . The dotted line is a trend line for
the plastic buckling of cell walls. This is non-linear, being negligible at low Vc (because there is no S2 cell wall layer), approximately linear between
Vc of 0.2±0.7 and dropping sharply at higher Vc (because there is no lumen for the S2 layer to buckle into). The solid line describes tissues with
only primary walls (,) and suggests little or no plastic work potential. The tissue with primary cell walls that has the highest Vc is collenchyma
dissected out from celery stalks (Apium graveolens L. var. dulce (Mill.) DC., Umbelliferae). The solid line intersects with a high-density seed shell
tissue. All the plastic work appears to be done within a 1 mm diameter circle around the crack tip. Multiplying the units of the vertical axis of E by
1 mm converts them to those of D. Then, the data points for the three woods in D can be slid across to E where they can be seen to ®t more or less
the dotted trend line. We conclude that plastic buckling seems to explain their toughness.
walls winding in the wall at a variable angle of about
15±308 to the long axis of the cell. This winding angle
causes the walls of any cell in the crack path to buckle
plastically into the lumen even under tension (Page et al.,
1971; Fig. 2B, C) and soak up much greater amounts of
energy (Gordon and Jeronimidis, 1980) than events within
the wall could alone. An estimate can be obtained by
plotting the gradients of toughness vs. specimen thickness
(when 50.5 mm) for all 82 tissues/materials. Figure 1E
shows this plotted against Vc . The contribution is very nonlinear, but dwarfs ®bre-based toughness in all tissues that
express it. It depends on the presence of secondary cell
walls, being almost non-existent for cells with only primary
walls and incipient in light wood with very thin secondary
walls (Fig. 2A). Plastic buckling also depends on the
presence of a cellular lumen and as Vc 4 1.0 in very dense
seed shells, the toughness increment associated with it drops
towards 0.0. The mechanism is therefore based in wall
structure and cellular geometry, something that is very
strongly supported by its e€ective temperature independence (Jeronimidis, 1980b), which is ecologically valuable in
its own right. Adding toughness contributions from Fig. 1D
to E gives a predicted maximal toughness of just over
30 kJ m ÿ2 for a plant tissue. This lies within the true realm
of tough materials. However, the mechanism can do more.
If the entire wall were wound as in the S2 layer, then a
model constructed by Gordon and Jeronimidis (1980)
proves that a toughness of 400 kJ m ÿ2 could be produced.
Some of the variation in Fig. 1E in the toughness of
woody tissues, at any given Vc , can be attributed to the
di€ering e€ectiveness of ®bres and tracheids. The latter have
a `multi-tasking' role, conducting sap as well as providing
Lucas et al.ÐMechanical Defences to Herbivory
917
F I G . 2. Scanning electron micrographs of four woods to show the in¯uence of structure on plastic buckling. A±C show wood surfaces that have all
been fractured by a crack travelling in a longitudinal-tangential direction. A, Balsa (Ochroma lagopus Sw. Bombacaceae) wood has too thin a
secondary cell wall to show much buckling. Many cells on this cut surface have retained their normal shape after fracture. In contrast, the thicker
walls of ®bres of both a tropical hardwood (BintangorÐCalophyllum sp. Guttiferae), shown in B, and C, a tropical softwood (Malayan KauriÐ
Agathis borneensis Warb. Araucariaceae) have buckled plastically to produce irregular cellular outlines after fracture. D, The wood of a climber
(Bauhinia sp.) has very large vessels which act to lower toughness to roughly half that of a tree wood of the same Vc (data point shown as an open
circle in Fig. 1E).
mechanical support, while ®bres are purely mechanical.
However, the proportion of vessels in hardwoods seems
more important. It seems likely that vessels either do not
buckle plastically or absorb little energy in doing so. The
purpose seems protective: sap ¯ow would be greatly
impaired if vessels collapsed. Angiosperms bene®t from
de-linking mechanical support from ¯uid conduction. There
is, generally, a higher volume fraction of vessels in temperate
woods than in tropical ones. A climber (Bauhinia sp.,
Caesalpinioideae, Bukit Timah, Singapore) has very large
vessels of about 0.3 mm in diameter occupying 50 % of its
volume (Fig. 2D). Both temperate hardwoods and this type
of tropical climber, which occupy a large proportion of their
cross-sectional area with vessels, may have reduced toughness compared to tropical hardwoods due to this e€ect.
Stress-limited defence
Cracks are always likely to start in a solid when a
particular stress is exceeded. Deterring herbivores from
reaching this stress level can be achieved by high hardness.
High hardness requires high density. While low-density
plant tissues tend to fail in a brittle manner, below their
yield stress (Vincent, 1990), high-density tissues could fail at
a multiple of up to three-times their yield stress like most
engineering materials (Wilsea et al., 1975). Unfortunately,
high density means that there is no space for cellular
contents. Thus, these dead, stress-limited, defences have to
be localizedÐusually, quite logically, on the outside of
plant tissuesÐas spines, prickles, thorns and hairs.
It is possible to build these structures simply with cells
that have very thick walls. The ®bres of many seed shells and
very dense woods have Vc 4 90 % and a maximal microhardness of around 300 MPa (Lucas, 1991; Lucas et al.,
1991, 1997). Since the axial compressive strength of the wall
of a wood ®bre is between 120±350 MPa (Gibson and
Ashby, 1997), this is probably the best that can be achieved.
A herbivore might be deterred if the hardness of its biting
apparatus were less than this. However, though 300 MPa
parallels the hardness of the sclerotized mandibles of insects
918
Lucas et al.ÐMechanical Defences to Herbivory
(Hillerton et al., 1982), it is low compared to the mineralized
dentitions of vertebrates, where the microhardness of
mammalian enamel is approx. 3500 MPa (Baker et al.,
1959; Waters, 1980). Thus, the sharp spikes that are typical
of such defences usually involve inclusions of amorphous
silica, of microhardness about 5000 MPa (Baker et al.,
1959). Named structures, such as spines and thorns (Grubb,
1992), refer to defences that humans can detect. Most of
those that we have looked at (with an EDX elemental probe
in a scanning electron microscope) contain silica, including
those on Alluaudia procera (Drake) Drake (Didiereaceae),
Aloe divaricata A. Berger (Liliaceae), Acacia bellula Drake
(Mimosaceae), Pachypodium rutenbergianum Vatke (Apocynaceae), Kalanchoe beharensis Drake (Crassulaceae) and
Commiphora simplicifolia H. Perrier (Burseraceae) collected
at Beza Mahafaly Reserve in the spiny dry forest of S.W.
Madagascar. Much smaller structures on leaves, often dismissed as hairs, do too, including Gluta wallichii (Hook. f.)
Ding Hou (Anacardiaceae) and Streblus elongatus (Miq.)
Corner (Moraceae) from Bukit Timah, Singapore (Lucas
and Teaford, 1995) and Celtis africana Burm f. (Ulmaceae),
Celtis durandii Engl. (Ulmaceae) and Ficus exasperata Vahl.
(Moraceae) leaves from Kibale forest, S.W. Uganda.
T H E R E PO R T E D E F F E C T I V E NE S S O F
THESE DEFENCES
A major problem with evaluating the e€ectiveness of plant
defences in the herbivory literature is confusion: a keyword
search for either `toughness' or `hardness' turns up a
multitude of papers that have not really researched either.
The state of the subject is, unfortunately, analogous to
bucket chemistry. This is a great pity because the energetic
approach of fracture mechanics in particular is ideally
suited to ecological investigations.
Most of the evidence for the importance of displacementlimited defences is indirect, generally from devices called
penetrometers that measure the force to push a circular ¯atended rod through a leaf. These devices are rarely described
in detail and the data produced with them are usually
treated more super®cially than chemical information.
Papers by Feeny (1970), Coley (1983) and Raupp (1985)
stand out among many that provide evidence that leaf
penetrometer forces re¯ect structural deterrents to invertebrate herbivores. However, Choong (1996) shows much
more by using a cutting test on Castanopsis ®ssa (Champ.
ex Benth.) Rehder & E.H. Wilson (Fagaceae) leaves. If
toughness is a deterrent to caterpillar consumption of this
species, then it appears to be generally protecting its
vascular system, particularly the beginning and end of the
midrib and secondary veins, and also the leaf margin. These
parts of the C. ®ssa leaf appear to have no chemical
defences. The latter are located mainly in the palisade and
spongy mesophyll of the lamina, where cells have to be
thin-walled to photosynthesize e€ectively and thus cannot
be mechanically defended. Parsimony in mechanical and
chemical defences seems barely explored.
A central tenet about the feeding selectivity of animals on
plants, with apparently strong supporting evidence, is the
avoidance of ®bre (e.g. in primatesÐMilton, 1979;
Waterman et al., 1988; Rogers et al., 1990). This is based
on the diculties of digesting ®bre, which optimization
studies suggest should be avoided (e.g. for mammalian
herbivoresÐAlexander, 1991). The problem, however, is
the sensible attributes that are available for its detection.
Toughness is sometimes treated as the physical equivalent
of ®bre. However, as detailed above (Fig. 1), this is false. If
it is agreed that the major detectable trait of the colourless,
odourless and tasteless cell wall, in the cellular context or
not, is its texture (Choong et al., 1992), then ecological
studies might do better to focus on toughness rather than
®bre. Hill and Lucas (1996) found that toughness explains
leaf food selection by Japanese macaques in Yakushima
better than neutral detergent ®bre content (were there to be
any other way of detecting this ®bre measure or its extracted
derivatives). More generally, Yamashita (1996) shows that
the diets of ®ve Malagasy lemurs can be characterized in
mechanical terms.
When ecologists speak of mechanical defences, they often
refer just to stress-limited defences. Many of these, such as
spines, thorns and the like, seem to be defences against
vertebrates (Grubb, 1992), including mammals of body size
ranging from woodrats (Cooper and Ginnett, 1998) to
gira€es and elephants (Young and Okello, 1998). Their
e€ectiveness is disputableÐsometimes because of the
extinction of many of the species of large mammal that
would otherwise explain their presence (Janzen and Martin,
1982). However, spines and thorns seem generally to reduce
the quantity of twigs or shoots eaten per unit of time by
vertebrate herbivores by reducing bite size (the volume of a
bite) or biting rate (Cooper and Owen-Smith, 1986;
Belovsky et al., 1991; Belovsky and Schmitz, 1994;
Gowda, 1996). A critical factor in the eciency of the
herbivore digestive system is the rate of passage of food
volume in the gut (Alexander, 1991). Experiments on
humans suggest that the optimum bite size is fairly large
(Lucas and Luke, 1984). Presuming the same to apply to
herbivores, then the e€ect of reducing bite size is likely to be
very signi®cant: spines and thorns help the plant lose less in
any herbivore encounter.
The scale of these defences seems too great to a€ect
invertebrate herbivoresÐe.g. Potter and Kimmerer's (1988)
study of Hyphantria cunea Drury (Lepidoptera) larvae
feeding on Ilex opaca Aiton (Aquifoliaceae) leaves. These
authors say, e€ectively, that the toughness of holly leaves is
a more likely deterrent than the leaf spines. However, in
many species, leaf hairs take over as a small herbivore
deterrent (Edwards and Wratton, 1980; Coley, 1983) by
functioning as tiny spines. The presence of silica in the hairs
of some species is further evidence of mechanical similarity
to spines. These hairs may be barely detectable to large
herbivores. As primate examples, in Bukit Timah, Singapore, long-tailed macaques, Macaca fascicularis Ra‚es
(Cercopithecidae) select G. wallichi and S. elongatus leaves
and, in Kibale Forest (Uganda), chimpanzees (Pan
troglodytes Blumenbach, Pongidae) feed extensively on
F. exasperata and C. africana leaves. C. durandii leaves are
the staple for black and white colobus monkeys (Colobus
guereza RuÈppell, Cercopithecidae) while red colobus (Piliocolobus badius Kerr, Cercopithecidae) feed on all three plant
Lucas et al.ÐMechanical Defences to Herbivory
species. All the above leaves in both sites are densely covered
with siliceous hairs at the age-stages eaten by these primates.
Hard structures like the above plant features are often
sharp because this makes optimum use of their localized
nature. They then behave like indenters, which will not
blunt themselves in contacts if their hardness is at least 2.5times that of their opponent. Wear is a complex subject but
abrasive wear appears to be largely the product of hardness
disparities. Amorphous silica in plants almost certainly
causes heavy tooth wear in grazing large herbivores (Baker
et al., 1959), but ungulates combat this to some extent by
producing high-crowned teeth. Grazing produces a very
scratched wear appearance on tooth surfaces of herbivores
compared to browsers (Walker et al., 1978), but this could
be reversed if, for example, tree leaves contained abundant
silica and if, in contrast, grasses accumulated most of their
silica in their roots (McNaughton et al., 1985). Silica, and
possibly calcium oxalate crystals (Danielson and Reinhard,
1998), widespread in angiosperms, could form more
common deterrents to leaf herbivores than is currently
realized via abrasion of biting surfaces.
Space (and references) limit a general discussion of which
aspects of plant structure are designed as mechanical
supports against the elements rather than defences to
herbivores. As a cell type, ®bres do both. It is the supracellular layout of the tissue that needs to be studied to decide
between these competing hypotheses. To take a speci®c
example, resistance to bending is optimized by a sandwich
construction with the sti€est elements (those with highest
Young's modulus) positioned close to the surface (Gibson
and Ashby, 1997). It is curious, in general, that most woody
®bres appear to have sacri®ced some sti€ness for toughness
in their constructionÐif cellulose micro®brils in the S2 layer
ran parallel to the cellular axis, sti€ness would be maximal
(and toughness, negligible). Certainly, the internal location
of these ®bres around veins in dicotyledonous leaves such as
C. ®ssa (Choong, 1996) is bad for preventing bending. Thus,
we vote for displacement-limited defences being just that.
However, the complex structure that is their vital element
takes time to develop and become e€ective. Any rapidly
developed tissue, plant or animal, tends to have poor
displacement-limited defences. Stress-limited defences are
much simpler to arrange.
AC K N OW L E D GE M E N T S
We thank the Research Grants Council of Hong Kong for
funding.
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