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First published online June 15, 2007
Journal of Experimental Biology 210, 2213-2230 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.001560
Review |
Techniques for predicting the lifetimes of wave-swept macroalgae: a primer on fracture mechanics and crack growth
1 Hopkins Marine Station of Stanford University, Pacific Grove, CA 93950,
USA
2 Department of Mechanical Engineering, Stanford University, Stanford, CA
94305, USA
* Author for correspondence (e-mail: mach{at}stanford.edu)
Accepted 8 April 2007
| Summary |
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Key words: fracture mechanics, breakage, fatigue, intertidal, macroalgae, seaweed, biomechanics
| Introduction |
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|
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Even though physical and physiological intertidal stresses are repetitive
in nature, associated with the flow and ebb of tides, most experiments have
focused on acute lethal stresses and repercussions for competitive ecological
interactions. Sublethal consequences of repeated desiccation, high and low
temperatures, hydrodynamic forces and other environmental conditions have
proven difficult to address (e.g. Koehl,
1984
; Koehl, 1986
;
Davison and Pearson, 1996
).
Here we describe methods for quantifying the potentially lethal effects of
repeated hydrodynamic forces.
| Hydrodynamic consequences for macroalgae |
|---|
|
|
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For seaweeds, hydrodynamic stresses imposed on thalli represent a
substantial facet of rocky shores' extreme physical environment. Subtidally,
water velocities reach several m s-1
(Denny, 1988
), while
magnitudes of water velocities increase manyfold intertidally (commonly to
1020 m s-1) as waves break and are funneled by substratum
topography (Denny et al.,
2003
; Denny,
2006
).
Intertidal macroalgae, as sessile organisms, cannot actively avoid the
violent water motion of the wave-swept environment. Instead, as water flows
past an intertidal seaweed, the water exerts force, primarily drag, on the
organism (Gaylord et al.,
1994
; Gaylord,
2000
; Boller and Carrington,
2006a
). Intertidal macroalgae thus experience forces,
predominantly in tension, throughout their lengths with each passing wave. And
macroalgae endure substantial forces: drag forces imposed by water moving at
10 m s-1 are comparable to the forces that would be exerted by
winds traveling at 1050 km h-1, nearly Mach 1, if air were
incompressible. Furthermore, intertidal seaweeds must endure these
hydrodynamic forces frequently; approximately 8600 waves break on shore each
day.
Many biomechanical studies have investigated the mechanical properties and
morphological attributes that enable wave-swept macroalgae to survive drag
forces imposed by breaking waves (e.g.
Carrington, 1990
;
Holbrook et al., 1991
;
Denny and Gaylord, 2002
;
Pratt and Johnson, 2002
;
Kitzes and Denny, 2005
;
Martone, 2006
). These studies
have investigated algal material properties primarily in tensile tests,
finding macroalgae highly extensible and generally compliant (the opposite of
stiff), with low breaking strength, compared to other biomaterials
(Hale, 2001
;
Denny and Gaylord, 2002
). In
addition, investigations have suggested the importance of algal flexibility,
which is in part a consequence of the compliance of algal materials. Seaweeds
align, deform and bundle with flow, thereby reconfiguring to reduce drag
(Vogel, 1984
;
Koehl, 1986
;
Boller and Carrington,
2006b
).
To date, studies of algal materials have evaluated their abilities to
resist large wave forces through pull-to-break tests, in which samples are
loaded in tension until they break. The force required for breakage,
normalized as stress (applied bulk force per initial material cross-sectional
area), is taken as the ultimate strength, or breaking stress, of the material.
This strength is then compared to the stresses imposed by the largest waves to
predict an alga's risk of breakage. These comparisons have repeatedly
predicted low probabilities of breakage (e.g.
Koehl and Alberte, 1988
;
Gaylord et al., 1994
;
Gaylord, 2000
;
Johnson and Koehl, 1994
;
Friedland and Denny, 1995
;
Utter and Denny, 1996
;
Denny et al., 1997
;
Johnson, 2001
;
Kitzes and Denny, 2005
),
leading to the suggestion that wave-swept algae are mechanically over-designed
(Denny, 2006
).
However, these predictions are at odds with reality: many seaweeds
experience consistent, substantial seasonal breakage and dislodgment
(Seymour et al., 1989
;
Dudgeon and Johnson, 1992
;
Dudgeon et al., 1999
;
Johnson, 2001
;
Pratt and Johnson, 2002
),
presumably due to wave-induced forces. For example, for two turf-like
intertidal macroalgae, Dudgeon and Johnson
(Dudgeon and Johnson, 1992
)
observed wintertime reduction in canopy cover reaching 13% for one species and
30% for another. In kelp forests, Seymour et al.
(Seymour et al., 1989
)
documented mortality ranging from 2 to 94% over four winter seasons. And the
sometimes meter-deep piles of seaweed washed up on beaches after storms stand
testament to frequent breakage and dislodgment.
Failure in seaweeds assumes a variety of forms. For example, breakage of
blades or load-bearing midribs may occur primarily at distal or marginal
regions. This `tattering' reduces the sizes of algal thalli
(Black, 1976
;
Blanchette, 1997
;
Dudgeon et al., 1999
) and
presumably lowers the risk of more catastrophic damage. Other seaweeds,
especially those with perennial holdfasts capable of regenerating stipes,
break primarily at the holdfast-stipe junction
(Carrington, 1990
;
Hawes and Smith, 1995
;
Shaughnessy et al., 1996
;
Carrington et al., 2001
;
Johnson, 2001
). For instance,
when experimentally pulling a turf-like red macroalga, Carrington
(Carrington, 1990
) found that
90% of thalli broke at the stipe-holdfast junction. Failure of this weak link
ensures survival of the holdfast and allows regeneration of stipes and blades.
Nonetheless, holdfast dislodgment, due to holdfast or substratum failure, does
occur frequently (Black, 1976
;
Koehl, 1986
;
Seymour et al., 1989
;
Utter and Denny, 1996
;
Gaylord and Denny, 1997
). For
feather-boa kelp (Egregia laevigata Setchell) washed onto beaches,
Black (Black, 1976
) documented
dislodgment due to holdfast or substratum failure for 35% of individuals, and
Koehl and Wainwright (Koehl and
Wainwright, 1977
) determined holdfast detachment responsible for
355% of dislodged and broken individuals of a subtidal kelp,
Nereocystis luetkeana (Mertens) Postels & Ruprecht, with tangled
plants more likely to fail at the holdfast.
In sum, although wave-swept macroalgae appear over-designed on the basis of measured algal strengths and maximal wave-induced stresses, breakage nonetheless occurs commonly at various locations on macroalgal thalli.
To account for the discrepancy between predicted and observed algal
breakage rates, several external factors, aside from maximum water speeds,
have been invoked. Studies have suggested that stipe entanglement, low-tide
physiological stress, senescence, water-propelled projectiles, and damage from
herbivory or abrasion may increase breakage beyond rates predicted on the
basis of maximum water velocities alone
(Friedland and Denny, 1995
;
Utter and Denny, 1996
;
Kitzes and Denny, 2005
;
Denny, 2006
). Along these
lines, two studies, for two different kelp species, linked herbivorous damage
to breakage in approximately 3050% of solitary individuals washed
ashore (Black, 1976
;
Koehl and Wainwright, 1977
),
and for the subtidal kelp N. luetkeana, Koehl and Wainwright
(Koehl and Wainwright, 1977
)
observed breakage at abraded locations on thalli in approximately 40% of
solitary individuals cast ashore. In addition, various researchers have
speculated that repetition of wave-induced stress, not just the
maximum stresses, may contribute to algal breakage
(Koehl, 1986
;
Hale, 2001
;
Kitzes and Denny, 2005
).
Experiencing in excess of 8000 waves per day, each with imposition of rapid
flow variation (Gaylord,
1999
), intertidal macroalgae may be weakened by the repeated
loading of stresses too low to break them in pull-to-break tests.
In this primer, we focus on the potential role of repeated loads in mechanical failure of wave-swept algae. Repeated loading may act in concert with damage initiated by abrasion and herbivory to cause breakage and dislodgment by fatigue.
| The role of fatigue |
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Most structural failures in human construction result from stresses well
below the ultimate material strengths of building materials. Consequently,
engineering theory includes a robust literature on crack formation through
fatigue and on growth of cracks introduced by fatigue or other means. We focus
specifically on fracture mechanics theory relevant to crack growth. Fatigue
has been evaluated, but not with fracture mechanics methods, in biological
materials ranging from bone to elastic proteins (e.g.
Caler and Carter, 1989
;
Currey, 1998
;
Keaveny et al., 2001
;
Gosline et al., 2002
). Failure
in the presence of cracks has been assessed using fracture mechanics in
biological materials such as bone, shell, horse hoof and grasses (e.g.
Behiri and Bonfield, 1984
;
Bertram and Gosline, 1986
;
Vincent, 1991
;
Kasapi and Gosline, 1996
;
Kuhn-Spearing et al., 1996
;
Kasapi and Gosline, 1997
;
Currey, 1998
;
Taylor and Lee, 2003
).
However, these biological studies involving fracture mechanics have focused on
the parameters relevant to propagation of cracks when materials fail
catastrophically in response to single loadings. Although gradual crack
extension may eventually cause complete fracture in conditions of repeated
loading, few biological studies have examined incremental crack growth at
sub-critical repetitively applied loads. Thus, studies to date do not address
our central question: can repeated loading of seaweeds lead to their
breakage?
Literature regarding fracture mechanics is almost exclusively written for specialized engineering audiences, and deciphering it, with the aim of applying it to biological situations, remains difficult for most biologists and even for many engineers. In response to the opacity of fracture mechanics literature, we provide here a coherent primer as a starting point for studies of fracture in organisms and as a strong basis for further investigation of the literature. To this end, we present a guide to relevant fracture mechanics techniques. We use consistent terminology for various fracture mechanics methods (a luxury often absent in the literature) and introduce relevant equations with intuitive explanations instead of extensive derivations. Interested readers are guided to cited literature for more detailed descriptions of equations' origins.
Although we use macroalgae as organisms of focus, presented techniques have
been applied, at least in part, to biological materials such as bone and horse
hoof (Behiri and Bonfield,
1984
; Bertram and Gosline,
1986
; Kasapi and Gosline,
1997
; Currey,
1998
) and are relevant to more extensible, softer biological
materials such as cnidarian mesoglea, arterial wall, skin, tendon and muscle
(Purslow, 1989
). We discuss
applied wave forces, but imposed stresses from any source can cause
repeated-loading damage. The accompanying article
(Mach et al., 2007
) tests the
feasibility of applying these techniques to several macroalgae.
We begin with two central parameters in linear elastic fracture mechanics
(LEFM), stress intensity factor and strain energy release rate, describing use
of these parameters as background for our presentation of techniques relevant
to flexible, extensible materials. [Readers interested in applying LEFM
techniques to botanical materials are referred to Farquhar and Zhao
(Farquhar and Zhao, 2006
).] We
then discuss strain energy release rate as it has been applied to fracture and
incremental crack growth in highly extensible elastomeric materials. Finally,
we discuss another parameter, the J-integral, that has been effective
in characterizing fracture and fatigue in materials not well described by LEFM
and fracture mechanics of elastomers.
For each fracture mechanics approach, we describe the methods used to evaluate the lifetime of a material with a crack of a particular size. That is, presented parameters enable estimation not only of the force necessary to fracture a specimen in a single loading, but also of the number of smaller repeated loadings that would eventually lead to fracture through incremental crack growth. We hypothesize that, by quantifying the effects of repeated loadings in this manner, we will be better able to predict algal breakage on wave-swept shores.
| Cracks reduce strength |
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In the following sections, we consider several types of stressstrain behavior, depicted in Fig. 1, where strain is the ratio of change in length to original length as stress is applied to a material (engineering strain). Linear elastic stressstrain behavior refers to materials with linear relations between stress and strain that return to their original length when unloaded (Fig. 1A). Non-linear elastic materials also recover deformations upon unloading but display non-linear relations between stress and strain (Fig. 1B). Finally, elasticplastic materials, upon loading, exhibit non-linear relations between stress and strain but additionally, upon unloading, leave irreversible deformation, termed plastic strain (or permanent set) (Fig. 1C). This plastic deformation exemplifies an inelastic strain.
|
Stress intensity factor is a parameter that, for linear elastic materials,
characterizes stress fields at very sharp crack tips. As an example, for a
sheet with an edge crack experiencing bending or axially applied stress
(Fig. 2A), the stress intensity
factor, KI (measured in
), can be expressed as:
![]() | (1) |
is the bulk tensile stress applied to the sheet, computed as if
no crack were present; a is a measure of crack length; w is
the width of the specimen; and f(a/w) is a
dimensionless function of the crack geometry and sheet width. For derivation
and further description of Eqn 1,
see elsewhere (Broek, 1982
![]() | (2) |
|
|
LEFM was originally developed for application to metals, in which concentrated stresses near crack tips cause plastic (permanent) deformations in tip vicinities. As long as plastic deformations are confined to a small zone around the crack tip, LEFM stress intensity factors, as well as strain energy release rate expressions described in the next section, can be applied to metals and other materials.
The critical value of stress intensity factor, KI, at which cracks advance is termed fracture toughness, KC. This critical value of stress intensity factor does depend on loading mode; KC here denotes fracture toughness for mode I loading. KC can be considered a material property in that it characterizes strength in the presence of a crack. As with properties such as ultimate tensile strength (breaking stress), fracture toughness typically varies with factors like temperature and rate of load application. For a given material, KC is approximately constant for different combinations of crack lengths and applied stresses, as well as for different specimen geometries, such as the examples shown in Fig. 2. KC is determined, using a relation such as Eqn 1, by measuring breaking stress for a material specimen of known dimensions, geometry and crack length. Once determined for one combination of specimen and crack geometry, KC can be applied to assess resistance to cracking for other geometries of the material.
With units of
, stress
intensity factors may seem abstract. A comparison between applied stress and
stress intensity factor may thus be helpful. When a specimen with no crack is
loaded, stress applied to the material can be measured easily. If the loaded
sample breaks in two, the stress at failure is a measure of ultimate tensile
strength. When the material contains a crack, however, due to variation of
stresses within the sample, the applied stress at failure will no longer be
constant for the material. Instead, stress at failure will vary with size and
shape of the crack as well as with geometry of the test specimen, with
geometry determined by relative specimen dimensions and crack location.
Consequently, in the case of a cracked specimen, stress intensity factor,
KI, instead of simply applied stress, can be used to
describe the physical state of the material. If the loaded sample breaks in
two, the pertinent parameter becomes not applied stress at fracture, but
stress intensity factor at failure, which is called fracture toughness,
KC. Thus, this geometry-independent term (fracture
toughness) is the material property preferred for characterizing loading in
materials with cracks.
Once determined for one combination of specimen geometry and crack size
(and given linear elastic conditions with limited crack-tip plasticity),
fracture toughness can be used to assess the reduction in a material's
strength for different specimen geometries and crack sizes. For
tensile-opening, mode I loading (Fig.
3A), the strength of the material,
C, is reduced
by the presence of a crack according to:
![]() | (3) |
LEFM, which includes stress intensity factors and
strain-energy-release-rate expressions described below, performs best for
materials such as glass and ceramics, which have little or no ability to
deform plastically and which have high moduli of elasticity (i.e. they are
stiff materials) and therefore experience relatively small bulk strains when
loaded to fracture. (Modulus of elasticity is the slope of a
stressstrain curve, with units of N m2.) For such
materials, strength reduction can be predicted reliably with
Eqn 3. For seaweeds, however,
large deformations act to round the crack tip and reduce stress
concentrations, thereby limiting the utility of linear elastic expressions in
predicting strength reduction in the presence of cracks
(Biedka et al., 1987
;
Denny et al., 1989
;
DeWreede et al., 1992
).
Crack-tip rounding ameliorates the strength reduction predicted by
Eqn 3. Nonetheless, cracks of
various geometries have been demonstrated to increase the likelihood of
breakage in several macroalgae (Denny et
al., 1989
; DeWreede et al.,
1992
).
In summary, stress intensity factor KI characterizes the stress field at a crack tip for linear elastic behavior, and fracture toughness KC quantifies the critical value of this factor at which a crack will propagate unstably to failure. Higher fracture toughness values occur in materials more resistant to fracture in the presence of cracks.
| Crack propagation |
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Consider a laboratory sample of an elastic material held by grips and pulled in tension to a fixed displacement. This fixed-grip condition can be used to explain another important concept: `strain energy release rate'. Work expended in extending the sample is stored as elastic strain energy, U, and no further work is done once the grips are stationary. Assuming no dissipative energy loss (e.g. through heat), the density of this stored energy, the elastic strain energy density (J m3), equals the area under the material's stressstrain curve at the fixed strain imposed by the grips.
Now, imagine introducing a sharp slit (or crack) into this extended
fixed-grip specimen. When the crack extends incrementally, creating new crack
surface dA, strain energy in material around the crack will relax,
causing the elastic energy stored in the specimen to decrease by dU.
This decrease in stored energy as new crack surface forms is known as the
strain energy release rate, G (J m2), given by:
![]() | (4) |
Some confusion in biological literature has arisen due to differing
definitions of dA (Biedka et al.,
1987
; Denny et al.,
1989
; Hale, 2001
).
Sometimes new crack surface area created in crack extension is taken to
include surface area of both faces of the crack, while at other times it
includes surface area on only one face of the crack. Here, dA refers
to newly created surface area on one face of the crack, and we encourage use
of this convention to standardize measurements.
For a central crack in a sheet (Fig.
2B) with length and width much greater than crack size, evaluating
Eqn 4 for mode I loading gives
strain energy release rate as:
![]() | (5) |
is the bulk stress applied to the specimen, a is half
the length of the central crack, E is the elastic modulus of the
material, and subscript `I' again indicates mode I, tensile-opening loading
(Broek, 1982Fracture testing usually involves pulling a cracked specimen while recording force-versus-displacement data. In such cases, strain energy release rate can be evaluated at displacements selected by the analyst, applying an experimental procedure similar to that introduced in Appendix A.
A crack will extend in a material when strain energy released in crack growth (expressed as a rate, dU/dA) exceeds energy required for the increase in crack surface area, dV/dA. The energy, V, absorbed during crack extension includes energy to create new surface as well as any energy dissipated through plastic deformation at the crack tip. The per-area rate at which energy is required for creation of crack surface, dV/dA, is often termed crack resistance, R.
Crack extension occurs when strain energy release rate, G, reaches a critical value GC equal to R. This crack advance may be stable or unstable. For example, when the driving force, G, for crack extension increases with crack growth, but crack resistance R remains constant, unstable growth occurs, which means that, once it begins to elongate, a crack will grow to specimen fracture. However, when R increases more than G with crack extension, stable crack growth occurs, in which crack extension occurs but does not lead to specimen fracture. In this scenario, a crack can advance a certain distance (while R<G) and then stop (when R>G), until higher loads are applied. Stable crack advance occurs mainly in materials that produce large plastic deformations with crack extension, such as thin plastic grocery bags, for which crack edges ruffle significantly during tearing, indicating plastic deformations. In most cases, GC, the critical strain energy release rate, corresponds to onset of unstable growth and fracture. Although we have described G here in terms of stationary grips to explicate the concept, GC in practice is usually determined by pulling specimens with initial cracks until unstable crack extension occurs.
We thus arrive at two different criteria for rapid crack propagation.
First, the stress intensity factor, KI, must equal
fracture toughness, KC. Second, the energy release rate,
GI, must have reached its critical value,
GC. For linear elastic materials, these criteria are
equivalent. From Eqn 2 and
Eqn 5, we can deduce that:
![]() | (6) |
![]() | (7) |
required for
fracture in the presence of this crack can be derived either by the
stress-intensity-factor approach (Eqn
1 or Eqn 2) or by the
strain energy release rate approach (Eqn
4 or Eqn 5). | Fatigue crack growth |
|---|
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In other words, for a macroalga with a crack, wave forces causing stresses
less than the material's ultimate strength in the absence of cracks, and less
than the applied stress required for complete fracture, may still cause crack
growth (that is, small increases in crack length) with each force imposition.
At a certain point, the alga's crack may grow to a length at which applied
wave forces reach GC and KC, leading
to the fracture described in the previous sections. As a result, examining
algal fracture in a manner that considers only maximum wave forces may neglect
breakage that will occur due to incremental crack growth during smaller,
repeated loadings. The curious, important phenomenon of `sub-critical' crack
growth can be characterized (although not mechanistically explained) using the
following LEFM procedure, which allows prediction of a material's lifetime in
conditions of repeated loading. The physical mechanisms for incremental crack
growth have been documented for some engineering materials but not for
macroalgae. For metals, for example, when a crack opens in response to
sub-critical bulk stresses, localized plastic straining at the crack tip
causes the tip to blunt on a microscopic scale, which elongates the crack a
small amount. Upon removal of the bulk stress, the crack tip re-sharpens with
increased length, iteratively elongating with repeated loading
(Pook, 1983
).
Predictions of specimen lifetimes proceed in two steps. First, baseline data are generated to describe the pattern of crack growth in a material. This baseline curve (Fig. 4) is then combined with real-world loading histories to predict time to failure.
|
From a curve fitted to a-versus-N data, crack
growth rates (mm cycle-1), da/dN, are calculated from the
curve's slope at different values of crack length, a. For each value
of crack length, a range of stress intensity factor,
KI, is computed from the range of applied stress,

(maximum stress minus minimum stress in a cycle), using a
relation such as Eqn 1. If the
minimum stress is zero, then
KI equals the maximum
value of KI applied in a cycle.
Crack growth rate values, da/dN, are then plotted against values
of stress intensity range,
KI, on logarithmic axes,
where
KI (for cyclic loading from zero to maximum
stress) equals the value of the stress intensity factor,
KI, at the maximum imposed stress
(Fig. 4). Each material has a
characteristic loglog plot of da/dN versus
KI, which often has the shape depicted in
Fig. 4. Growth rate generally
increases with increasing crack length and with increasing applied stress. At
low
KI, crack growth is extremely slow, and there
is sometimes a threshold value of
KI below which no
crack growth occurs (Broek,
1982
), shown as
KTH in
Fig. 4. Similar baseline curves
can be generated for other loading modes
(Fig. 3) as well.
Lifetime
Once baseline data are generated, lifetime of a cracked material in
repeated loading conditions can be determined. Determination of lifetime
requires a loading history, a plot of stress applied to a material over time.
The loading history is analyzed to predict when fracture will occur, that is,
when KC or GC will be reached. There
are multiple approaches to this calculation. In one common LEFM approach,
crack growth is assumed to occur only during rising, tensile ranges of loading
(Nelson, 1977
). In other
words, crack growth is assumed to occur only while applied stress stretches a
specimen beyond its initial length, not while specimen extension decreases in
tension and not while a specimen is loaded in compression. In the loading
history, each time that applied tensile stress increases from one value to
another and then drops, that increase (or range) of stress is considered
equivalent to a loading cycle used in generation of the baseline
da/dN-versus-
KI curve
(Fig. 4).
For each successive rising tensile range in a loading history or in a
representative sequence of loading, crack growth for that cycle is added to
current crack length. The increment of crack growth for the cycle,
da/dN, corresponds, on the baseline data plot (i.e.
Fig. 4), to the stress
intensity range
KI of the tensile loading. As
subsequent stress impositions are analyzed, crack length increases, and when
the stress intensity range reaches fracture toughness, fracture is predicted
to occur. In other words, the critical crack length corresponding to
GC or KC for the applied stress has
been reached, and material rupture is predicted, as long as resistance to
fracture, R, does not increase significantly with crack extension, as
described in the previous section. In this fashion, the number of loadings to
failure, or lifetime, of the cracked material is estimated.
In sum, to apply this procedure to a seaweed, one experimentally generates
a baseline curve describing crack growth in response to repeated loading in a
macroalga containing cracks, i.e. a
loglogda/dN-versus-
KI curve
(Fig. 4). Each species, and
perhaps each population, requires a separate baseline curve characterizing its
crack growth behavior. Then a history of imposed wave forces is converted to
imposed wave stresses through consideration of a macroalga's cross-sectional
area. For each rising tensile imposition of stress in this wave stress
history, the calculated range of applied stress, 
, combined with
crack length, a, can be used to determine
KI for the loading (e.g.
Eqn 1). Then, for each rising
stress imposition, the corresponding crack growth is determined from
KI for the stress imposition and from the
corresponding da/dN in the baseline data curve. When crack length is
sufficient for
KI to equal KC,
breakage of the alga is predicted.
The power of this procedure is that breakage of seaweeds can be examined in a manner that considers each force imposition (each wave) that seaweeds experience. It thus estimates the lifetime of a cracked alga as number of waves required for a crack to grow to failure.
In general, crack growth in engineering materials involves substantial
variability (Broek, 1982
), and
differences between predicted and actual growth result from variability in
material cracking and fracture behavior, as well as from idealizations and
simplifications in prediction methods. Similar variability likely occurs for
macroalgae.
LEFM may not effectively characterize algal fracture. Because LEFM performs
best for materials displaying brittle fracture (which seaweeds often do not,
compared to engineering materials), alternative methods should be explored,
and two such approaches are described below. Even if other methods are found
superior for application to seaweeds, LEFM might be well applied to some plant
materials such as leaves and wood
(Farquhar and Zhao, 2006
) or
to shells to predict cycles to failure during predator loadings (e.g.
Boulding and LaBarbera, 1986
;
LaBarbera and Merz, 1992
) or
wave force impositions.
| Crack growth in macroalgae |
|---|
|
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|---|
|
Strain energy release rate, T, may be found experimentally, as for
linear elastic materials, by loading specimens with initial cracks until
cracks extend unstably (Appendix A). Critical values of TC
defined by these loadings are analogous to GC for linear
elastic materials. Experimental results demonstrate that
TC is approximately constant for different specimen and
crack geometries and therefore can be considered a material property
characterizing resistance to fracture
(Rivlin and Thomas, 1953
;
Thomas, 1994
). Thomas
(Thomas, 1955
;
Thomas, 1994
) also showed
that T can be related to W, the strain energy density around
the surface of a crack tip of diameter d:
![]() | (8) |
is the angle shown in Fig.
6 and W(
) indicates that W is a function
of
. Thomas determined this relation by considering a specimen's change
in energy with an increment of crack extension, which is dominated by elastic
strain energy relaxed in a small zone ahead of the crack tip
(Thomas, 1994
|
Single-edge-crack specimens
For rubber specimens each with a single edge crack (e.g.
Fig. 2A), pulled in tension,
energy release rate is given by:
![]() | (9) |
(Rivlin and Thomas,
1953
at
=1, then drops to approximately 1.6 at
=3. Numerical
analysis confirmed these results (Lindley,
1972
can be adequately
approximated by the simple relation:
![]() | (10) |
To determine critical energy release rate, TC, a single-edge-crack specimen with crack length a is stretched until it breaks, and force and extension at fracture are measured. Wo in Eqn 9 can be found from the stressstrain curve of a specimen without a crack; Wo is the area under that stressstrain curve up to the bulk stress at which fracture occurred in the cracked specimen.
Trouser-tear specimens
Another common method for determining TC of rubber-like
materials involves trouser-tear specimens
(Fig. 7). A trouser-tear
specimen consists of a rectangular sheet cut along its long axis to form a
pants-shaped test piece. The `legs' are pulled in opposite directions to
create tearing action (Fig.
3C). Greensmith and Thomas
(Greensmith and Thomas, 1955
)
note the convenience of this test piece, for which TC and
rate of tear propagation are independent of crack length.
|
For trouser-tear tests, critical energy release rate can be found from:
![]() | (11) |
is extension ratio in the legs during tearing, F is
force applied to the legs during tearing, b is initial thickness of
the test piece, Wo is strain energy density in the legs
during tearing, and C is initial cross-sectional area of both legs
combined, the cross-sectional area of the `body' of the test piece
(Rivlin and Thomas, 1953
![]() | (12) |
, expended in loading, tearing, and unloading
of a specimen, obtained from the area under a forcedisplacement plot
(e.g. Fig. 8). Then, critical
energy release rate is given (Purslow,
1983
![]() | (13) |
ab is the crack extension surface area, taken as
distance traveled by a crack between its initial and final lengths,
a, multiplied by thickness of a specimen, b.
Fluctuations in force with crack extension of the kind illustrated in
Fig. 8 are typical of
variations observed for macroalgae as well as other pliant biological tissues
(Purslow, 1989
|
Biedka et al. (Biedka et al.,
1987
) and Denny et al. (Denny
et al., 1989
) determined critical strain energy release rates for
seaweeds from trouser-tear tests using formulations similar to
Eqn 12 and
Eqn 13 except that they
referenced fracture energy to two times the fracture surface area. They termed
the measured property `work of fracture', even though they measured critical
energy release rate. Multiplying their works of fracture by two (and again by
two for Denny et al.'s values to account for a spurious factor introduced in
their calculations) yields critical strain energy release rates for seaweeds
comparable to calculations from Eqn
12 and Eqn 13.
Center-crack specimens
For another specimen geometry, a center-cracked specimen
(Fig. 2B), strain energy
release rate for tensile-opening loading
(Fig. 3A) is given by:
![]() | (14) |
) varies, strictly speaking,
for center-crack (Eqn 14) and
edge-crack (Eqn 9 and
Eqn 10) specimens because
deformation of an edge crack is less constrained, as discussed, for example,
by Sanford (Sanford, 2003
In the linear elastic case, Eqn
14 is equivalent to the LEFM expression for G
(Eqn 5). Under elastic
conditions, strain energy density, Wo, is area under a
stressstrain curve. Under linear elastic conditions, this area under
the curve, and thus strain energy density, equals
2/2E. In addition, for linear elastic conditions,
specimen extensions are usually small compared to elastomer extensions, so
that 
1. Substitution of these values yields
![]() |
Effects of viscoelasticity
Many elastomers, as well as macroalgae, display some degree of viscoelastic
behavior, a combination of elastic and time-dependent viscous
stressstrain behavior. As such, they violate the assumption of
elasticity inherent in the analyses so far.
Viscoelastic behavior is characterized, for example, by stresses relaxing
if material is moderately stretched and held fixed or by inelastic (creep)
strains developing if material experiences constant load over time. Under
constant-amplitude, cyclic loading, viscoelastic behavior appears in loops
formed by stressstrain curves for repeated loading and unloading cycles
(e.g. Fig. 9, as compared to
elastic behavior shown in Fig.
1A,B). Viscoelastic loadingunloading loops displayed by
seaweeds (Fig. 9A) resemble
loops exhibited by rubbers (Fig.
9B). Often, for elastomers and macroalgae, loop width decreases
with repeated cycles and tends towards much smaller values for lower specimen
extension (e.g. Fig. 9). In
addition, a residual inelastic (plastic) strain may remain after the first
cycle, but additional increments of residual strains often become negligible
(Fig. 9). Similar
stressstrain behavior has been observed in other plant tissue
(Spatz et al., 1999
) and in
muscle of soft-bodied arthropods (Dorfmann
et al., 2007
). This viscoelastic behavior will be most pronounced
in crack-tip regions where stresses and strains are much higher than in the
bulk of the specimen.
|
T, has been used successfully to correlate crack growth
rate under zero-to-tension repeated loading in rubber
(Lake, 1995
K has been used successfully in linear elastic analyses.
Since the value of T at the maximum point of a load cycle is
T when the minimum point is zero (no extension), T
will be used here without
.
Characterizing crack growth rate
As with LEFM analyses, crack growth per cycle of loading, da/dN,
may be evaluated in a nonlinearly elastic material over a range of strain
energy release rates, T (Atkins
and Mai, 1985
; Lake,
1995
; Seldén,
1995
). Then, the relationship between da/dN and
T is determined. The cyclic crack growth per cycle is represented as
some simple function of T, a relationship often maintained over a
wide range of crack growth rates:
![]() | (15) |
When f(T) is known, incorporating effects of specimen
shape and applied forces, this equation can be used to predict crack growth
rate behavior for a given material, analogous to data presented in
Fig. 4. For specimens each with
a single-edge crack (Fig. 2A),
cycled in tension, energy release rate is described by
Eqn 9. For this equation, for a
cyclically loaded sample, Wo is taken as the strain energy
density at maximum extension,
max. Wo
is often measured directly from stressstrain plots for un-notched
samples, assuming that regions far from a crack behave as if no crack were
present (Atkins and Mai, 1985
).
Likewise, k is calculated for
max. Calculated
T is plotted versus da/dN, as done for
KI data (Fig.
4).
For crack extension in regions of intermediate-to-high strain energy
release rates, crack growth rate per cycle commonly follows an empirically
determined power-law form (Lake,
1995
; Seldén,
1995
):
![]() | (16) |
Predicting lifetime
Eqn 16 can be integrated to
determine the number of loading cycles, N, required for a crack to
grow from length a1 to length a2.
Consider the case of a single-edge-cracked specimen
(Fig. 2A) that experiences
cyclic loading with constant maximum extension. From
Eqn 9, T in
Eqn 16 is set equal to
2kWoa. Eqn
16 then becomes
![]() |
![]() |
![]() | (17) |
![]()
![]() | (18) |
This equation allows for powerful predictions [see accompanying article
(Mach et al., 2007
)]. Once
baseline crack-growth behavior of an alga has been evaluated with
Eqn 16,
Eqn 18 can be used to estimate
the number of waves of a certain magnitude required to break an edge-cracked
alga through incremental crack growth. That is, for a flat-bladed alga with an
edge crack, Eqn 9 can be used
with stressstrain curves to determine the wave force required to
fracture the alga in a single wave, once critical values of T have
been measured. Eqn 18, in
contrast, enables prediction of the wave force required to break an
edge-cracked alga in, for example, 100, 1000 or 10 000 waves, thereby
estimating lifetime of the notched alga in different wave conditions. Wave
force can then be correlated with offshore wave height, given various
assumptions about wave breaking (Gaylord,
1999
; Denny et al.,
2003
; Helmuth and Denny,
2003
; Denny,
2006
), allowing predictions of the frequency with which notched
algae experience waves sufficient to break them in these 100, 1000 or 10 000
wave loadings.
| J-integral and elasticplastic fracture |
|---|
|
|
|---|
|
J has been found useful in analyzing resistance to crack extension
in materials with extensive plastic deformation emanating from crack tips. The
critical value of J at which onset of crack extension occurs,
JC, can be considered a material property. Like fracture
toughness KC, JC is in principle
independent of specimen and crack geometry as well as crack size. Over the
years, J has been applied successfully as a fracture parameter for
metals and plastics (Kim et al.,
1989
; Bose and Landes,
2003
; Wainstein et al.,
2004
).
J can be interpreted graphically
(Fig. 11). Suppose test
specimens with two different crack lengths, a and (a+da),
are pulled to a fixed displacement. The area between the curves for two
different crack lengths (Fig.
11) represents the change in stored energy, dU, that
occurs for crack extension da. dU is (Jtda), where
t is specimen thickness and dA=tda
(Broek, 1982
). For this fixed
displacement example,
![]() | (19) |
|
Note that energy release rate usually involves energy released from a
specimen to `feed' a growing crack in elastic material. If large amounts of
plastic deformation occur when a cracked specimen is loaded, much energy
absorbed by the specimen is not recovered upon unloading or crack advance
(Anderson, 2005
). In such a
situation, Eqn 19 relates
J to the difference in energy absorbed by identical specimens with
two different crack sizes.
Although derived for non-linear elastic behavior
(Fig. 1B), J can be
applied to the loading portion of an elasticplastic stressstrain
curve (e.g. Fig. 1C). The
J-integral is not defined for unloading. Nevertheless,
J has been successfully correlated with crack growth rate,
da/dN, for repeated cycles of loading and unloading
(Dowling and Begley, 1976
)
even when gross amounts of plasticity accompany crack growth. With such
correlations, J can be used, as described for G and
T, to predict lifetime of materials with cracks, including
seaweeds.
Furthermore, for some elastomeric materials and certain specimen designs,
energy dissipates during specimen deformation and does not contribute to
cracking processes. This dissipated energy should be separated from energy
that contributes to cracking in determining fracture resistance. J
may provide a means of partitioning energy in the crack-tip region from energy
dissipated in the bulk of a specimen (Lee
and Donovan, 1985
).
Because it accommodates non-linear stressstrain curves and extensive plastic deformation at crack tips during loading, J may be another fracture parameter that could be fruitfully applied to macroalgal fracture processes.
| Conclusions |
|---|
|
|
|---|
Furthermore, the methods presented from LEFM, fracture mechanics of elastomers and elasticplastic fracture mechanics enable prediction of the lifetime for breakage of other biological materials with cracks or flaws in the presence of isolated large loads or of repeated loadings. Although incremental crack growth at sub-critical loads has been largely ignored for many biological materials, such fatigue crack growth may contribute importantly to ecologically, evolutionarily and physiologically relevant breakage in organisms ranging from seaweeds to terrestrial plants to animals.
| Appendix A |
|---|
|
|
|---|
(m), the difference between specimen length at a given time and initial
specimen length (Fig.
A1A).
|
For a selected value of specimen displacement,
*, a plot
of stored strain energy U (J) versus initial crack length is
constructed (Fig. A1B). Given
elastic material behavior, stored strain energy is the area under the
loaddisplacement curve, in this case between zero displacement and
* (Fig.
A1A). If unstable tearing occurs before a specimen reaches the
selected displacement, the specimen's loaddeformation curve in
Fig. A1A is extrapolated to
estimate stored energy.
Then, a third plot (Fig.
A1C) of specimen displacement at tearing versus initial
crack length is generated from the loaddisplacement plots in
Fig. A1A. From this plot, for
the displacement selected for Fig.
A1B,
*, one determines initial crack length,
a*, for which tearing would have occurred at the given
displacement from a line fitted to the data points. At this value of
a*, the tangent to the
U-versus-a curve
(Fig. A1B) is determined. This
tangent (or slope) yields dU/da, which can be converted to
critical strain energy release rate, TC, or
dU/dA, by multiplying the tangent by
1/specimen thickness. Any selected value of specimen displacement for
construction of the second plot (Fig.
A1B) should yield approximately the same value of
TC.
| Appendix B |
|---|
|
|
|---|
![]() | (A1) |
is a path-independent, counterclockwise contour surrounding a
crack tip, W is strain energy density, and P is a stress
vector acting on an element of path length ds
(Fig. A2A). P is
defined according to the outward-direction, unit-vector normal to
,
n (Fig. A2A; see
Eqn A2 and
Eqn A3 below). In
Fig. A2A, u denotes a
vector quantifying displacement of the material at the same location
(ds), while (
u/
x) is a
displacement gradient (see Eqn
A4 and Eqn A5
below). Although the stress (traction) vector is usually notated with
`T', here we use `P' to avoid confusion with strain energy
release rate T.
|
x,
y, and
xy, acting on a small element of material
(Fig. A2B). The
x and
y components elongate (or compress)
material, while the
xy component shears material. Also for
illustration, a rectangular contour
around a crack tip will be
considered, depicted in Fig.
A2C.
The traction vector P can be expressed as
Pxi+Pyj, where i
and j are unit vectors in the x and y directions,
respectively. Px and Py can be found
from:
![]() | (A2) |
![]() | (A3) |
xy and
Py=
y. Along 23,
(nx, ny)=(1, 0), so that
Px=
x and
Py=
xy. Along 34,
(nx, ny)=(0, 1) so that
Px=
xy and
Py=
y. Along 45 and 61,
(nx, ny)=(1, 0), yielding
Px=
x and
Py=
xy.
Deformation of an object is commonly represented by a displacement vector
that describes the change in coordinates of a point in the object, from
(x1, y1) to (x2,
y2). The vector is given by:
![]() | (A4) |
![]() | (A5) |
Forming the scalar product
P·(
u/
x) along segment 12
yields
![]() |
![]() |
Each segment will contribute to the J-integral as indicated in Table A1. Note that along this rectilinear path ds becomes either dx or dy, depending on the segment.
|
The strain energy density term along a segment can be evaluated for
two-dimensional stress from
![]() | (A6) |
x,
y, and
xy are
normal (
) and shear (
) strain components present along a segment.
Integration is carried out from the initial state (no strains) to the final
state (maximum strains reached).
Several approaches exist for evaluating the terms in the
J-integral when significant plastic straining is present. For
example, the displacement terms
u/
x and
v/
x, as well as
u/
y and
v/
y, can
be found by optical methods such as Moire interferometry
(Dadkhah and Kobayashi, 1990
),
digital image correlation (Sutton et al.,
1991
), and electronic speckle pattern interferometry
(Moore and Tyrer, 1994
).
Corresponding strains can then be computed from
x=
u/
x,
y=
v/
y and
xy=
[(
u/
y)+(
v/
x)].
From a material's stressstrain curve, stress components
x,
y and
xy can be
computed from these strain components using relations between stresses and
strains available from the theory of plasticity
(Sutton et al., 1996
;
Chakrabarty, 2006
). If a
contour is taken far enough from a crack-tip region to make plastic straining
negligible, simpler linear elastic stressstrain relations can then be
used (Kawahara and Brandon,
1983
). Determination of the variation of displacements, strains
and stresses along the segments of the contour provides input to the
evaluation of the terms in the line integrals in
Table A1. The variation of a
given term (e.g. W) along a segment can be fitted by a mathematical
function of x or y to facilitate integration
(Read, 1983
).
The J-integral may also be determined using commercially available finite element programs that compute the terms involved in the integral from loads applied to a given specimen geometry, without the need for experimental data other than a stressstrain curve.
List of symbols and abbreviations
Equation in which each symbol is first used is given (if symbol is used in an equation).

J
KI
KTH
T



max

xy


C



| Acknowledgments |
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