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Wood Biomechanics and Anatomy of Pachycereus pringlei

Article  in  American Journal of Botany · May 2000

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American Journal of Botany 87(4): 469–481. 2000.

WOOD BIOMECHANICS AND ANATOMY OF

PACHYCEREUS PRINGLEI1
KARL J. NIKLAS,2,4 FRANCISCO MOLINA-FREANER,3
CLARA TINOCO-OJANGUREN,3 AND DOMINICK J. PAOLILLO, JR.2
2Department of Plant Biology, Cornell University, Ithaca, New York 14853-5908 USA; and
3Instituto de Ecologia UNAM, Apartado Postal 1354, Hermosillo, Sonora CP83000, Mexico

We report the longitudinal, biomechanical, and anatomical trends observed for tissue samples drawn from the parallel
aligned, prismatic woody vascular bundles running the length of a Pachycereus pringlei plant measuring 5.22 m in height.
The main vertical stem of this plant was cut into five segments (labeled A through E in the acropetal direction) measuring
;1.02 m in length. Four of the 14 vascular bundles in each segment were surgically removed to obtain 20 vascular bundle
segments that were tested in bending to determine their stiffness measured in the radial ER and tangential ET direction. We
also determined the lignin content of representative samples of wood.
A nonlinear trend in stiffness was observed: ER and ET were highest in segments B or C (1.67 GN/m2 and 1.09 GN/m2,
respectively), lower in segment A (ER 5 1.18 GN/m2 and ET 5 0.35 GN/m2), and lowest in segment E (ER 5 0.03 GN/m2
and ET 5 0.20 GN/m2). Similar longitudinal trends were seen for axial tissue volume fraction and fiber wall thickness, which
achieved their highest values in segment B (69.8% and 6.59 mm, respectively). Wood stiffness also correlated significantly
with cell wall lignin content: with respect to segment B (which had the highest lignin content, and was thus used as the
standard reference for percent lignin content), lignin content, was 15, 60, 85, and 43% in segments E, D, C, and A,
respectively. Fiber cell length, which increased toward the base of the stem and toward the vascular cambium in the most
proximal vascular bundle segment, did not correlate with ER or ET.
Basic engineering principles were used to calculate stem stresses resulting from self-loading and any wind-induced bending
moment (produced by drag forces). Calculations indicated that the less stiff wood produced in segment A eliminates a rapid
and potentially dangerous increase in stresses that would otherwise occur in segments B or C. The less stiff wood in segment
A also reduces the probability of shear failure at the cellular interface between the wood and surrounding tissues in this
portion of the stem.
We conclude that P. pringlei wood stiffness is dependent on the volume fraction and lignification of axial tissues, less
so on fiber wall thickness, and that wood development in this species is adaptively responsive to self-loading and differ-
entially applied external mechanical forces

Key words: biomechanics; Cactaceae; lignin; plant stems; Young’s modulus; vascular tissues; wind drag; wood.

Based on an examination of two plants, the stiffness
of wood samples drawn from the vascular bundles run-
ning the length of Pachycereus pringlei (Cactaceae)
stems is reported to vary nonlinearly, such that wood
achieves its maximum stiffness near but not at the stem
base of this species (Niklas, Molina-Freaner, and Tinoco-
Ojanguren, 1999). Although this trend is somewhat coun-
terintuitive, because bending stresses achieve their max-
imum intensities at the base of any vertical structure
(Wainwright et al., 1976; Niklas, 1992), the amount of
wood produced in P. pringlei stems increases basipetally
such that the flexural rigidity (i.e., the ability to resist
bending forces) increases exponentially toward the base
1 Manuscript received 20 April 1999; revision accepted 27 July 1999.
The authors thank Prof. James D. Mauseth (University of Texas) who,
as an Associate Editor of the American Journal of Botany, supervised
the reviewing process and served as Editor-in-Chief for this manuscript;
the owners of El Sacrificio who provided access to their property; Ivan
Romo for logistical support; Recardo Clark, Daniel Morales, Grethel
Ramirez, and Martin Villegas for assistance in the field; and Prof. P.
Schopfer (Institut für Biologie II der Universität, Freiburg) for sharing
his expertise in lignin analyses. Field work was supported by funds from
the operating budget of the Instituto de Ecologis UNAM to FMF. This
research was also supported by Hatch Act Awards 185-403 (KJN) and
185-406 (DJP), and a von Humboldt Forschungspreis (KJN).
4 Author for correspondence (phone: 607 255 8727; FAX 607 255
5407; e-mail: kjnz@cornell.edu).
469
of stems due to an increase in the axial second moment
of area, which increases as the third or fourth power of
transection size. Nonetheless, no mechanical explanation
was offered for the adaptive (if any) role of less stiff
wood near the base of P. pringlei stems, and, despite
detailed anatomical reviews of the Cactaceae (Gibson,
1978; Gibson and Nobel, 1986), no anatomical infor-
mation that could account for the nonlinear trend in wood
stiffness was available. Variation in a number of anatom-
ical features is known to influence (or at least correlate
with) plant tissue stiffness, which is generally assumed
to increase with the volume fraction of cell wall materi-
als, cell wall lignification, and symplast turgor pressure,
and assumed to decrease with fiber cell length and the
volume fraction of air-filled spaces (Record, 1934; Falk,
Hertz, and Virgin, 1958; Seibt, 1964; Carlquist, 1975;
Wainwright et al., 1976; Niklas, 1992). However, in the
absence of detailed study, the specific anatomical fea-
ture(s) possibly accounting for the trend in P. pringlei
wood stiffness remain(s) problematic.
In this paper, we re-examine the longitudinal variation
in P. pringlei wood samples drawn from another repre-
sentative plant in the context of a detailed anatomical and
biomechanical investigation. Our objective was to deter-
mine whether the previously reported trend in wood stiff-
ness could be reproduced, and, if so, to determine which
470 AMERICAN JOURNAL
among the contending anatomical features of the wood
could account for this trend. The biomechanical protocol
previously used to investigate the longitudinal variation
in P. pringlei wood was repeated using the main vertical
stem of a plant comparable in height and diameter to
those of the two previously examined plants. The stem
of the newly examined specimen was dissected as were
the previous two stems to remove representative and
widely spaced woody vascular bundles that were then
individually tested in bending to determine their bulk tis-
sue stiffness (Young’s modulus E) measured in the radial
and tangential directions with respect to the grain of the
wood. Smaller but anatomically representative tissue
samples were removed from some of the tested bundle
segments and anatomically and biomechanically exam-
ined to determine which among the many tissue proper-
ties were correlated with wood stiffness.
Another objective was to determine whether self-load-
ing and external environmental factors may influence the
properties of P. pringlei wood along the axis of the stem
by indirectly affecting the development of the derivatives
of the vascular cambium. Any columnar stem exerts com-
pressive stresses on its tissues and is subject to chronic
mechanical perturbation, which is known to alter stem
and leaf morphology and tissue stiffness (see Telewski,
1995, and references therein). It is possible, therefore,
that the development of P. pringlei stem wood is influ-
enced by the magnitudes of the stresses generated by the
increasing weight of the stem and by periodic or aperi-
odic mechanical disturbance, both of which have the po-
tential to alter the anatomy and thus the mechanical prop-
erties of wood. Since the vascular cambium is located
away from the centroid axis of the stem where bending
stresses reach high (but not their highest) levels and since
the magnitude of these stresses measured at the same lo-
cation with respect to the center of a vertical stem gen-
erally increases toward the base of a columnar support
member, we speculated that self-loading and differential
wind-induced bending stresses may serve as develop-
mental cues for a longitudinal variation in wood stiffness,
especially since stem growth in height is determinate for
this species. This hypothesis, which was not tested di-
rectly for technological reasons, was examined indirectly
by calculating the stresses experienced by the intact P.
pringlei stem resulting from its weight and wind acting
normal to the stem surface.
The data and calculations we present are argued to
provide strong circumstantial evidence that P. pringlei
wood stiffness is significantly and positively correlated
with the volume fraction and the extent of lignification
of axial tissues, less so with fiber wall thickness, and not
at all with fiber cell length, which varies across tissue
samples in the conventional manner for woody species.
Our calculations likewise provide good evidence that
self-loading and wind-induced stem flexure influence the
development of wood such that the less stiff and more
extensible wood prevents abrupt increases in axial com-
pressive stresses and reduces the probability of shearing
failure at the interface between any two tissues differing
in their material properties (i.e., wood development in
this species is adaptively responsive to self-loading and
differentially applied external mechanical forces).
OF BOTANY [Vol. 87
MATERIALS AND METHODS
Study site and plant selection—The field site was on a west-facing
bajada of the Sierra Seri located at Rancho El Sacrificio (29E 05.829N,
112E 08.009W), which is in the coast of the state of Sonora, Mexico,
in an area that belongs to the Central Gulf Coast vegetational subdivi-
sion of the Sonoran Desert (Shreve, 1964; Felger and Moser, 1985).
The plant selected for study measured 5.22 m in height and ;0.21 m
in basal stem diameter, and differed in no noticeable way from conspe-
cifics of similar size. It was selected for study because of its healthy
appearance and size, which was intermediate between two previously
examined specimens (measuring 3.67 m and 5.89 m in height), for
which we have biomechanical data (see Niklas, Molina-Freaner, and
Tinoco-Ojanguren, 1999).
Dissection protocol—The main stem of this plant was cut into five
stem segments of nearly equivalent length (;1.02 m). These segments
were labeled A–E in an acropetal sequence from the base to the top of
the stem. The outlines of the transverse surface of each segment and of
each of the 14 vascular bundles running the length of entire segment
and of each of the 14 vascular bundles running the length of entire stem
were drawn to scale for future reference. The cut ends of each segment
were also labeled to record their proximal-distal orientation, and indi-
vidual vascular bundles were assigned consecutive numbers (1–14),
which were consistent among the five stem segments. Each stem seg-
ment was then dissected to remove its vascular bundles for mechanical
testing. During this process, the smaller lateral strands joining the larger
neighboring vascular bundles were purposefully broken and removed to
obtain prismatic beams that were, on average, 1.02 m long.
The five prismatic segments of each of four vascular bundles (num-
bers 2, 5, 9, and 13) were tested in bending (N 5 20 vascular bundle
segments). These four vascular bundles were selected for detailed study
because they were located at the corners of an imaginary square drawn
on the transverse surface of each of the five stem segments. Prior re-
search indicated that the cross-section geometry and size of vascular
bundles can vary as a function of location in tilted or curved stems.
Even though the stem studied here appeared to be perfectly vertical,
this protocol was used to avoid as best as possible any bias in tissue
stiffness resulting from wood developing under the influence of tensile
or compressive stresses.
Biomechanical protocol—Bending tests were used to determine the
vascular bundle tissue stiffness (Young’s modulus E) measured in the
radial and tangential directions (ER and ET, respectively). The flexural
rigidity EI of each tissue sample was also determined. Young’s modulus
E is a measure of the ability of a material to resist bending; it is a size-
independent parameter. Flexural rigidity EI is a measure of the ability
of a structure to resist bending; it is a size- and shape-dependent pa-
rameter because the second moment of area I is a measure of the con-
tribution made by the transverse geometry and size of the material used
to fabricate a structure to the ability of the structure to resist bending.
The determination of E and I is necessary therefore because the material
properties and transverse shape and size of vascular bundles are not
uniform throughout the stems of P. pringlei. Pristmatic segments from
each of the four vascular bundles were placed between two vertical
supports and then loaded by placing bags of sand varying in weight
attached at the midlength of each segment. A horizontally oriented nee-
dle was sighted against a metric ruler to measure the midlength vertical
deflection d resulting from the load. Young’s modulus was computed
from the formula E 5 PL3/48dI, where P is a mass-force of the load
and L is the free length of the vascular bundle segment. Second mo-
ments of area were computed on the basis of morphometric measure-
ments of transections taken at the bottom, middle, and upper thirds of
each sample. Different formulas for I were used depending on the trans-
verse geometry of the tissue samples and the orientation of the sample’s
cross section with respect to the plane of bending (see Fig. 3). For
April 2000] NIKLAS ET AL.—CACTUS WOOD BIOMECHANICS
further details, see Niklas, Molina-Freaner, and Tinoco-Ojanguren
(1999).
Anatomical protocol—After the bending tests were completed, short
(;8 cm) segments of tissues were removed from the middle, upper, and
lower thirds of each vascular bundle segment and preserved in FAA
(formalin–acetic acid–ethanol) for subsequent anatomical study in the
laboratory.
Three vascular bundles (2, 5, 13) of the four bundles tested biome-
chanically were evaluated for features of the axial and radial systems.
In bundle 5, coordinated sampling furnished information on volume
fraction of axial vs. ray systems, volume fraction of fibers, fiber wall
thickness, and fiber and vessel element cell length. Bundles 2 and 13
were used as replicates for determining the volume fraction of axial vs.
ray systems. In the context of the vascular cylinder of the plant, bundles
2 and 5 were separated by two intervening bundles, as were bundles 2
and 13.
Bundle 5 furnished transverse sections (20–80 mm thick), taken on a
sliding microtome, from samples at the midregion of each segment, A–
E. One set of sections were stained with phloroglucinol-HCl to develop
pink to red coloration in lignified cell walls, and photographed with a
digital camera and transmitted light to produce prints at ;103 magni-
fication. The photographic print of each section (or the montage in the
case of a larger section) was photocopied, the photocopy was divided
into ray system vs. axial system using scissors, and the relative pro-
portions of the two systems by weight was taken as an indication of
their volume fractions.
Using an arbitrary band width that was fully occupied by the sec-
ondary xylem of segment E, photocopies of segments A–D were divid-
ed into strips parallel to the locus of the vascular cambium, so that
volume fractions of axial and ray systems could be estimated as a func-
tion of distance from the cambium. The layer closest to the cambium
was designated as layer 1.
Other sets of transverse sections were stained with 1% toluidine blue
in water, dehydrated, and mounted in synthetic resin. Digital photo-
graphs (at 2303) taken through the microscope were assembled as mon-
tages to record images of the axial system in each segment in transverse
section along the radius. Photocopies of these assemblies were used to
separate pore space and associated parenchyma cells from the ground-
mass of fibers, so that relative abundance of fibers could be estimated
at the midpoints of segments A–E along the axis, and along the radius
of segment A, as was done for the relative abundance of the axial
system itself.
Fiber wall thickness was measured on digital photographs (7403)
taken with the microscope from transverse sections to evaluate layer 1
in segments A–E. A minimum of 250 measurements was taken from
the sample for each segment. Wall thickness was measured from the
middle lamella to the lumen at approximately two locations for each
cell that was evaluated.
Finally, for bundle 5, samples of wood for macerations were taken
from locations near the midline of the bundle for evaluation of cell
lengths. After treatment with macerating fluid, the 2-cm long samples
were stained in bulk with 1% basic fuchsin in 95% ethanol. As a basis
for replication of the measurements of the lengths of fibers and vessel
elements, three fragments of wood were selected from separate locations
in a sample and prepared as three separate slides by dehydration, dis-
section, and mounting in synthetic medium.
Cell lengths were measured using a 103 lens of the compound mi-
croscope, which just accommodated the longest fibers in the field of
view, and a drawing tube positioned above a digitizing tablet under the
control of a microcomputer. Typically 80–95 cells were measured on
each slide. Fibers were measured from tip to tip in layer 1 of segments
A–E, and at six equally spaced locations along the centerline of segment
A, across layers 1–13. Vessel element lengths were measured in layer
1 of segments B and E. Measurements were from the center of the
transverse to oblique perforation plate at one end to the center of the
471
perforation plate at the opposite end of the cell, to exclude as much as
possible the effect of apical intrusive growth on the length of vessel
elements.
For bundles 2 and 13, in each of the five 8-cm samples from the
midregion of segments A–E, the two transverse ends were ground
smooth with Carborundum papers and photographed in reflected light
with a 35-mm camera. Photographs at ;103 were photocopied, and
the relative proportions of axial vs. ray system were estimated as for
bundle 5 (above), but using both ends of a sample to estimate volume
fractions, as a function of distance along the axis. Bundle 13 furnished
small beams that were used in additional bending experiments. The
beams were selected to represent six locations spanning the radius of
segment A, with three replicates from layer 1. Each end of each beam
was photographed using a stereomicroscope, and photocopies of prints
at 253 were used to determine volume fraction of axial vs. ray systems,
as above.
Lignin analysis protocol—The lignin content of wood samples was
analyzed using the protocol of Müsel et al. (1997) modified after Bruce
and West (1989). Wood samples weighing 8 g were removed from the
8 milled prismatic beams taken from segment A and from the most
recently formed growth layers in segments B–E (all samples were from
vascular strand 13). Each sample was frozen in liquid nitrogen for ;60
s, pulverized, and subsequently thawed in 2.0 mL homogenization buff-
er (50 mmol/litre Tris-HCL, 10 g/L Triton X-100, 1 mol/L NaCl; pH
8.3). The suspension was vortexed and then centrifuged (at 2000 g for
10 min). The recovered cell-wall pellet was washed twice with 4 mL
of the homogenization buffer, 80% acetone, and pure acetone, and sub-
sequently lyophilized. Each pellet was then treated with 0.4 mL thiogly-
colic acid 1 2 mL 2 mol/L HCl for 4 h at 958C, after which it was
centrifuged (at 15 000 g for 10 min) and washed three times with dis-
tilled water. The lignothioglycolic acid (LTGA) from each pellet was
extracted with 2 mL 0.5 mol/L NaOH (agitating for 16 h at 208C); the
supernatants (collected after a first and second centrifugation during
which the pellets were re-extracted with 0.8 mL NaOH) were combined
and acidified with 0.4 mL concentrated HCl. LTGA was precipitated
for 3.5 h at 48C, recovered by centrifugation (at 15 000 g for 20 min),
and dissolved in 1 mL 0.5 mol/L NaOH. Aborbance was measured
against a NaOH blank in the range of 220–320 nm. The amount of
lignin was calculated from the aborbance at 280 nm using a specific
absorbance coefficient of 6.0 L·g21·cm21 using a conversion to relative
units based on the relationship: absorbance of 100 mg lignin in 1 mL
5 0.60 A280 in a 1-cm cell. Because the 6.0 L·g21·cm21 specific absor-
bance coefficient is an approximate conversion (the absorbance of
LTGA from different sources can vary considerably; see Doster and
Bostock, 1988), the specimen with the highest lignin content among the
12 samples (i.e., the wood removed from segment B) was used as an
internal standard to express the percent lignin content of the other wood
samples.
Stress and bending moment computations—We calculated the
stresses produced by the weight of stem tissues (self-loading, compres-
sive stresses) based on the formula si 5 [S (r·g·Ai·,i)]/{Ai 1 [(Es/Ec 2
1)As]}, where r is the bulk stem tissue density, g ; 9.8 kg·m21·s22, ,i
is stem length measured from the top of the stem (where ,i 5 0), Ai is
stem cross-sectional area at i, Es is vascular strand stiffness at i, Ec is
bulk stiffness of the nonwoody tissues at i, and As is the combined cross-
sectional area of all vascular strands at i (see Timoshenko and Gere,
1961; Lin and Burns, 1981; Niklas, 1992). The term S (r·g·Ai·,i) com-
putes the ‘‘running sum’’ of stem weight above any cross section i; the
term {Ai 1 [(Es/Ec 2 1)As]}, or ‘‘the transformed-section,’’ is the stem
cross-sectional area adjusted for the relative stiffness and cross sectional
area of the vascular strands with respect to those of their surrounding
tissues (see Appendix). A numerical value of Ec 5 0.115 GN/m2 was
used (i.e., the average wood stiffness measured for segment E); how-
472 AMERICAN JOURNAL OF BOTANY [Vol. 87

ever, any value for Ec obtains the same relative stress magnitudes pro-
vided that Ec is more or less constant along the stem.
We modeled the effects of hypothetical longitudinal variations in vas-
cular strand stiffness on stem self-loading stresses by stipulating that Es
increases linearly from the top to the bottom of the stem based either
on the measured stiffness of the strands segments A, D, and E (model
1) using the linear regression formula Es 5 0.86 2 0.15 d, where d is
distance from ground level, or the wood stiffness measured for segments
B, C, D, and E to predict the stiffness of the wood in segment A (model
2) using the linear regression formula Es 5 0.2.02 2 0.41 d. Model 1
predicts less stiff wood for segments B and C; model 2 predicts higher
wood stiffness in segment A than that which actually occurs. In tandem,
the two models define the lower and upper limits for the longitudinal
wood stiffness gradient that was actually observed.
In order to evaluate the consequences of wind-induced stem flexure,
we measured stem diameter di at different distances xi from the top of
the stem (x 5 0), and computed the surface area each stem element i
(any imaginary section of the stem with finite length) projected toward
the on-coming wind as the product of its diameter di and effective length
xi 2 xj (where xj denotes the distance from the tip of the stem to the
top of the element i). The drag force Df acting at the base of element i
resulting from a wind speed u acting normal to the stem surface was
then computed from the formula Df 5 0.5rui2 [di·(xi 2 xj)]CD, where r
is the density of air (taken as 1.205 kg/m3) and CD is the drag coefficient
(taken as 1.0). A logarithmic wind speed profile was used to specify
values of ui at different heights above ground such that the maximum
wind speed occurred at the top of the stem utop (arbitrarily set equal to
10 m/s) and progressively decreased to zero at ground level, i.e., the Fig. 1. Mean 6 SE of wood stiffness (Young’s modulus E) mea-
wind speed profile was calculated on the basis of the formula, ui 5 sured in the radial and tangential directions (ER and ET, respectively)
[utop/ln(h/zo)] ln[(h 2 xi)/zo], where h is the height of the cactus stem plotted as functions of the location of five segments (segments A–E) of
(;5.2 m) and zo is the roughness height (set equal to 0.75 m based on four vascular bundles with respect to the top of the Pachycereus pringlei
the surrounding vegetation). The magnitude of the drag force acting stem.
locally on any stem element i thus decreases toward the base of the
stem but the bending moment and stresses it creates increase basipetally
toward ground level. The bending moment Mi resulting from the drag secondary xylem had accumulated. Wood stiffness mea-
force for any element i was computed on the basis of the formula sured in the radial direction was greatest in segment B
(mean 6 SE 5 1.67 6 0.35 GN/m2) the midpoint of
Mi 5 O {0.5ru [d ·(x 2 x )]C }x .
i

j51
2
i i i j D i
Bending stresses were computed on the basis of the formula si 5
d iMi/2Ii 5 32Mi/pd 3i .
Statistics—ANOVA and Model Type I and II regression analyses
were used to determine whether E or EI varied significantly and pre-
dictably as a function of distance from the top of the stem and to de-
termine the extent to which biomechanical and anatomical parameters
were correlated. Given the objectives of this study, we emphasized sta-
tistical comparisons between wood stiffness measures in the radial and
tangential directions and the volume fraction of axial tissues, fiber wall
thickness, and fiber cell length. All analyses were performed using the
software package JMPq(SAS Institute, Inc.) on a Power Macintosh
8100/80.
RESULTS
General biomechanical phenomenology—The bio-
mechanical properties observed during our study of the
third P. pringlei stem do not differ in any substantive
way from those previously reported for two other stems
examined from this species (Niklas, Molina-Freaner, and
Tinoco-Ojanguren, 1999).
Tissue stiffness measured in either the radial or tan-
gential direction increased from the top to the base of
each bundle but decreased near the base of the stem in
either segment A or B (Fig. 1), where large quantities of
which was located ;1.5 m from ground level; wood stiff-
ness measured in the tangential direction was greatest in
segment C (mean 6 SE 5 1.09 6 0.16 GN/m2) the mid-
point of which was located ;2.5 m from ground level.
The disparity between the locations where the stiffest
wood measured in the radial and tangential direction was
found (segment B and C, respectively) may be a conse-
quence of experimental error resulting from difficulties
in orienting the larger vascular bundle segments with re-
spect to the direction of the bending force. Anatomical
observations indicated that the axial and ray tissue sys-
tems of the older parts of vascular bundles ‘‘fan’’ outward
toward the vascular cambium when viewed in the trans-
verse plane (Fig. 2); this anatomy is more reliably ori-
ented (and thus more reliably tested in bending to deter-
mine its stiffness) with respect to a radial rather than a
tangential acting bending force.
Despite the apparent discrepancy between where radial
and tangential wood stiffness reached their maximum
values with respect to location from the top of the stem,
a statistically significant and positive correlation was
found for ER and ET: r 2 5 0.55, P . ztz 5 0.002 (Fig. 3).
Reduced major axis (Model Type II) regression analysis
showed that tangential wood stiffness increases at a slow-
er rate with respect to rate at which radial wood stiffness
increases (i.e., aRMA 5 DET /DER 5 0.49). On average, the
stiffness of the wood measured in the radial and tangen-
tial direction was 0.94 6 0.17 GN/m2 and 0.56 6 0.08
April 2000] NIKLAS ET AL.—CACTUS WOOD BIOMECHANICS 473

Fig. 2. Transverse sections of wood showing the alternation of ray and axial tissues. (A) Sample from segment A. Rays (lighter) and axial
tissues (darker with light vessel lumens) fan outward in the section. Number of alternating panels increases outward with the formation of new rays
from within the axial system. Bar 5 10 mm. (B) Sample from segment E at the same magnification (see bar in A) shows difference in size and
overall morphology of the bundle as seen in transverse section at the two locations. At this level of sampling no new rays have originated and
divergence in the outward direction is limited. (C) Vessel elements (V) in the axial tissue (A) are embedded in paratracheal parenchyma and a
matrix of thick-walled libriform fibers. Rays (R) are composed of relatively thin-walled parenchyma cells. Bar 5 100 mm.

GN/m2, respectively (N 5 20). The wood was thus me-
chanically anisotropic in its behavior (i.e., its resistance
to a bending force depended markedly on the direction
of an externally applied bending force; see Niklas, Mo-
lina-Freaner, and Tinoco-Ojanguren, 1999).
The flexural rigidity EI of the vascular bundles in-
Fig. 3. Wood stiffness (Young’s modulus E) measured in the tan-
gential direction (ET) plotted as a function of wood stiffness measured
in the radial direction (ER) for 20 segments isolated from four vascular
bundles of a Pachycereus pringlei stem. Solid line and formula are for
ordinary least squares regression analysis.
creased exponentially toward the base of the stem and
was significantly larger when measured in the radial than
in the tangential direction (Fig. 4). The exponential in-
crease in flexural rigidity was attributed to the accumu-
lation of wood in older portions of the vascular bundles
and the attending increase in the axial second moment of
area I. The higher values for EI measured in the radial
direction as opposed to the tangential direction was at-
tributed to the, on average, greater stiffness of the wood
measured in the radial direction, and to the fact that the
cross-sectional shapes of the vascular bundles tended to
be more amplified in the radial than in the tangential
direction as wood is added over the course of growth and
development (Fig. 2A, B). Calculations (not shown) re-
vealed that the mechanical anisotropy of the wood (i.e.,
ER . ET) was not the over-riding factor in determining
differences in the flexural rigidity measured in the radial
and tangential directions (i.e., changes in cross-sectional
shape and size attending the accumulation of wood in the
vascular bundles had the largest influence on differences
in EI).
Anatomical and biomechanical relationships—Trans-
verse sections showed that the alternating panels of ray
and axial tissues increase in number outward, in a pattern
consistent with the origin, over time, of new rays within
the axial system (Fig. 2A, B). The axial system contained
474 AMERICAN JOURNAL
Fig. 4. Mean 6 SE of flexural stiffness (EI) measured in the radial
and tangential directions (EIR and EIT, respectively) plotted as functions
of the location of five segments (segments A–E) of four vascular bun-
dles with respect to the top of the Pachycereus pringlei stem. Shaded
outlines, which are drawn to scale, represent transverse geometries of
representative segments; orientation of these sections correspond to the
direction of the applied bending force used to measure E, which is here
arbitrarily defined in the vertical direction with respect to each graph.
solitary and clustered vessels with paratracheal parenchy-
ma in a matrix of libriform fibers, whereas the massive
rays consisted of relatively thin-walled parenchyma cells
(Fig. 2C). The occurrence of smaller diameter vessel el-
ements that clustered as coincident tangential bands in
adjacent panels of axial tissues indicated the presence of
growth layers. However, the spacing between successive
bands was not entirely regular, and the environmental fac-
tors that may be responsible for the layering have not
been determined (e.g., fluctuations in water availability
or temperature).
Layering was best expressed in samples from the distal
segment of the axis. It was confirmed that the spacing
and degree of differentiation of layers were duplicated
among bundles in the distal segment, and that the layers
expressed therein were represented by corresponding lay-
ers that were somewhat more weakly expressed in the
more proximal segments of the axis.
The volume fraction of axial tissues (expressed as a
percentage of the total wood volume) varied along the
radial transect through the various wood growth layers
within any one vascular bundle segment. The highest per-
cent volume fraction determined any where in one seg-
ment occurred in the youngest wood nearest the vascular
cambium. In segments C, D, and E, the lowest percent
volume fraction of axial tissues occurred in the oldest
wood farthest away from the vascular cambium, but, in
segments A and B, the oldest wood had a percent volume
OF BOTANY [Vol. 87
Fig. 5. Relationship between the percent volume fraction of axial
tissues in wood and relative distance d of wood sample from the vas-
cular cambium for five segments (A–E) drawn from a vascular bundle
of a Pachycereus pringlei stem. The cartoon shown at lower right of
figure denotes the transverse geometry of segment A and shows the
relationship between d and the vascular cambium at the top of the
cartoon.
fraction of axial tissues that was slightly higher than
wood nearer to the vascular cambium (Fig. 5). The per-
cent volume fraction of axial tissues determined along
much of the radial transect through the wood in segment
A was numerically equivalent to the percent volume frac-
tion determined for axial tissues in segment E.
The mean percent volume fraction of axial tissues de-
termined for all the wood in any one segment varied as
a function of distance from the top of the stem in a man-
ner similar to that observed for the radial and tangential
wood stiffness (Fig. 6A). That is, both the percentage of
axial tissues and wood stiffness reached their global max-
imum values in segment B. Statistical comparisons, how-
ever, indicated that the numerical value of this anatomical
parameter is not significantly greater in segment B com-
pared to segment C (P , 0.10), whereas it is significantly
greater in both segments B and C compared to segment
A. Fiber wall thickness in the outermost (youngest) layer
of the wood (i.e., wood layer 1) also peaked in segment
B (Fig. 6B). Statistical comparisons indicated that this
anatomical parameter differed significantly between seg-
ments A and B and between B and C but not between
segments A and C. Although the variances are large, the
average fiber wall thickness was less in segment A than
in either segment B or C.
The relative abundance of fibers showed no trend along
the lengths of the vascular bundles and no trend along a
radial transect though the various wood layers of segment
A (data not shown). In the youngest wood (layer 1), fiber
length was longest in segments A and B and declined
through segment E, and fiber length declined inward in
segment A (data not shown). This result indicates the
classic relationship that cell length increases with the
‘‘age’’ of the cambium in secondary xylem (Dinwoodie,
1961). To show that the axial differences were not due
April 2000] NIKLAS ET AL.—CACTUS WOOD BIOMECHANICS 475

Fig. 6. Mean 6 SE of percent volume fraction of axial tissues (A)

and fiber wall thickness t (B) plotted as a function of the location of
five segments (A–E) drawn from four vascular bundles of a Pachycer-
eus pringlei stem. For further details, see text.
Fig. 7. Mean wood stiffness measured in the radial and tangential
directions (ER and ET, respectively) plotted against mean percent volume
fraction of axial tissues (A) and mean fiber wall thickness (B) deter-
mined for corresponding tissue samples. Solid lines and formulas are
for ordinary least squares regression analyses.

simply to greater apical intrusive growth in the segments

with longer fibers, we also compared vessel element thickness 3 percent axial tissue volume was found to be
lengths more or less exclusive of apical intrusive growth. statistically significant at the 5% level.
The ratio of lengths within cell types in layer 1 of seg- Bending experiments on eight carefully milled small
ments B vs. E is essentially the same for vessel elements prismatic beams, which were surgically removed from six
as for fibers (1.3 vs. 1.4). Thus, we concluded that the different locations in section A of bundle 13, obtained
longer fibers represent the products of longer initial cells values for wood stiffness that were strongly correlated
in the cambium. with the percent volume fraction VR of axial tissues in
Model Type I regression analyses indicated that the the beams. Ordinary least squares regression indicated
mean values for wood stiffness (measured in the radial that ER 5 22.97 1 0.06 VF (r 2 5 0.98) and ET 5 22.48
and tangential directions) measured for large segments of 1 0.05 VF (r 2 5 0.95) (Fig. 8). There was no evident
the vascular bundles significantly correlated in a positive
and linear manner with the mean percent volume fraction
of axial tissues (despite the small sample size; N 5 10),
but the wood stiffness did not correlate with the mean
values of fiber wall thickness (Fig. 7A and B, respec-
tively). Based on analyses of residuals and R2 values,
multiple regression analyses confirmed that mean fiber
wall thickness detracted from rather than augmented the
ability to predict wood stiffness based on the joint op-
eration of mean percent axial tissue volume and mean
fiber wall thickness. We note, however, that the failure to
find a statistically significant correlation between wood
stiffness and fiber wall thickness or a correlation between
wood stiffness and the joint effects of these two anatom-
ical parameters was principally due to the higher than
expected value observed for fiber wall thickness in seg- Fig. 8. Stiffness (Young’s modulus E) measured in the radial and
ment E (see Fig. 6B). When the data point representing tangential directions (ER and ET, respectively) for small, milled prismatic
samples of wood isolated from segment A (the most proximal segment)
the mean fiber wall thickness in segment E was removed of a Pachycereus pringlei vascular bundle plotted as a function of per-
from our regression analyses, the correlation between cent volume fraction of axial tissues. Solid lines denote ordinary least
wood stiffness and either fiber wall thickness or fiber wall squares regression curves for these data.
476 AMERICAN JOURNAL OF BOTANY [Vol. 87

correlation between the location of each tissue sample

and its stiffness or volume fraction of axial tissues (data
not shown). Two samples had the same VF and wood
stiffness; yet, these two tissue samples were located at
the opposing ends of the radial transect through section
A. These experiments on beams of wood with precisely
defined and uniform second moments of area confirmed
the hypothesis that wood stiffness is positively and lin-
early correlated with the percent volume fraction of axial
tissues, that, on average, ER . ET, and that the wood
stiffness is not directly affected by location with respect
to the vascular cambium.

Lignin content of wood samples—The lignin content

of wood samples removed from the eight milled prismatic
beams isolated from segment A and from the most re-
cently formed wood in the growth layers of segments B–
E (all from strand 13) and the volume fraction of axial
tissues in each sample were linearly and positively cor-
related (r 2 5 0.98, n 5 12). Statistical comparisons
among the regression parameters for the samples re-
moved from segment A and from segments B–E indicat-
ed that the trends for lignin content and axial tissues for
the two different categories of wood samples did not dif-
fer significantly (Fig. 9A).
The stiffness measured in the radial and tangential di-
rection for the milled wooden beams and the average
wood stiffness in segments B–E was positively and lin-
early correlated with lignin content (r 2 5 0.82 and 0.83,
respectively) (Fig. 9B). The predictability of wood stiff-
ness improved when cell wall lignin content was included
with the volume fraction of axial tissues in multiple re-
gression analyses (e.g., R2 5 0.91 vs. r 2 5 0.82 for radial
wood stiffness; R2 5 0.89 vs. r 2 5 0.83 for tangential
wood stiffness). Also, since the lignin content in wood
growth layers of equivalent age in segments A–B varied
as did the percent volume fraction of axial tissues (Fig.
9C), we concluded that P. pringlei development is ca- Fig. 9. Relationships among percent volume fraction of axial tis-
pable of differentially adjusting these two parameters as sues, wood stiffness (Young’s modulus), and wood lignin content for
the inner derivatives of the vascular cambium mature and tissue samples from eight milled prismatic beams of wood removed
that variations in cell wall lignin content and percent vol- from segment A and for the most recently formed wood in segments
ume fraction of axial tissues affect wood stiffness differ- B–E. (A) Percent volume fraction of axial tissues plotted as a function
ently (i.e., the lignin content of cell walls and volume of lignin content expressed as a percentage of the absolute lignin content
of the youngest wood produced in segment A (percent lignin content).
fraction of axial tissues in wood are correlated, but these (B) Wood stiffness measured in the radial and tangential direction plot-
two variables are not autocorrelated to the degree that ted against percent lignin content. Solid lines are ordinary least squares
wood stiffness can be predicted exclusively on the basis regression curves. (C) Percent volume fraction of axial tissues and per-
of one or the other variable). cent lignin content of wood samples drawn from the most recently
formed growth layers in segments A–E plotted as a function of segment
Self-loading and wind-induced bending stresses— location along stem length. See text for further details.
The magnitude of the stresses resulting from the self-
loading computed on the basis of the actual stiffness of
the vascular strands (see Fig. 1) and their combined for the flexural rigidity of the vascular strands EI and the
cross-sectional areas increased in a basipetal direction self-loading stresses computed on the basis of the empir-
and, neglecting the solid woody base of the stem, reached ically determined values for wood EI (Fig. 10B), whereas
maximum intensity in segment A (Fig. 10A). In contrast, the correlations between EI and the stresses predicted by
two models, each of which stipulated a basipetal but lin- models 1 or 2 were significantly less strong (r 2 # 0.63).
ear increase in wood stiffness such that the stiffness of The less stiff wood produced in segment A (or, converse-
the wood in segments B and C was underestimated (mod- ly, the more stiff wood produced in segments B and C)
el 1) or the stiffness of the wood in segment A was over- thus obviated a steep ‘‘stress-rise’’ anywhere along the
estimated (model 2), predicted that the self-loading length of the stem and the resistance afforded by the vas-
stresses would reach their maximum in either segment B cular strands to bending under the stem’s self-load was
or segment C (models 1 and 2, respectively) (Fig. 10A). proportional to the stresses resulting from self-loading.
A statistically strong, exponential relationship was found Wind-induced bending stresses were two orders of
April 2000] NIKLAS ET AL.—CACTUS WOOD BIOMECHANICS
Fig. 10. Self-loading stresses and flexural rigidity of vascular
strands. (A) Self-loading stresses in stem segments A–E plotted as a
function of distance from ground level. Actual stresses (bold curve) for
segments A–E computed on the basis of the empirically determined
longitudinal variations in the stiffness of the vascular strands using the
formula shown at upper right. The stresses resulting from models 1 and
2 are based on the assumption that wood stiffness increases linearly
toward the base of the stem. Model 1 is based on a linear regression
formula using the stiffness of wood in segments A, D, and E; model 2
is based on a linear regression formula using the stiffness of wood in
segments B–E. Both models predict that self-loading stresses will reach
their maximum intensity in stem segments other than segment A. (B)
Flexural rigidity of the vascular strands measured in the radial and the
tangential directions plotted as a function of the actual self-loading
stresses (data taken from Fig. 10A; see bold curve). Solid lines are
ordinary least squares regression curves. For further details, see text.
magnitude greater than the stresses resulting from axial
compression (self-loading). Calculations indicated that
the bending stresses and the wind-induced moment
achieve near maximum intensity (;98%) at the top of
segment A and that the maximum rate of change of the
bending moment and stresses occur at the midspan of
section B (Fig. 11A). The statistically strong relationship
(r 2 5 0.99) between the vascular strand EI and the wind-
induced bending stresses was log-log linear. A strong
positive correlation was also observed between EI and
the magnitude of the bending moment M at different lo-
cations along the length of the stem (Fig. 11B). Finally,
a significant positive correlation existed between wood
stiffness measured in either the radial or the tangential
direction and the rate of change of the bending moment
(r 2 $ 0.78) (Fig. 11C).
DISCUSSION
Wood stiffness and anatomy—The relationship be-
tween the anatomical and mechanical properties of plant
477
Fig. 11. Relationships among bending moment M and rate of
change of the bending moment DM with respect to distance from ground
level d and between mean wood stiffness measured in the radial direc-
tion ER and the bending moment and the rate of change of the bending
moment computed for the Pachycereus pringlei stem from which wood
samples were examined. (A) Bending moment and rate of change of
the bending moment (computed on the basis of morphometric measure-
ments of the diameter and effective length of stem elements and a cur-
vilinearly decreasing wind profile) plotted as a function of distance from
ground level. The distance of the midpoints of vascular bundle segments
A–E are indicated for reference. Solid curved line connects the points
at which the bending moment was actually computed. (B) Flexural ri-
gidity EI measured in the radial and tangential directions at the mid-
points of segments A and B plotted as a function of the bending moment
(see Fig. 11A). (C) Wood stiffness measured in the radial and tangential
directions (ER and ET, respectively) plotted as a function of the rate of
change of the bending moment computed at the midpoints of vascular
bundle segments A–E. Solid line denotes linear regression for mean
wood stiffness; thinner lines are regression curves for ER and ET.
tissues has been the subject of considerable attention be-
cause, in addition to its physiological function(s), every
tissue type provides some measure of mechanical support
against the effects of gravity or wind movement
(Schwendener, 1874; Carlquist, 1961, 1969, 1975; Esau,
1967; Wainwright et al., 1976; Niklas, 1992; Mauseth,
1988; Speck, 1994; Spatz et al., 1995). Prior studies show
that a number of anatomical features influence the me-
chanical properties of any particular tissue, and that, all
478 AMERICAN JOURNAL
others things being equal, tissue stiffness is positively
correlated with the apoplastic volume fraction and degree
of cell wall lignification (Forsaith, 1929; Record, 1934;
Carlquist, 1975; Seibt, 1964; Niklas, 1992).
The present study provides additional support for the
hypothesis that the bulk stiffness of wood increases in
proportion with the apoplastic volume fraction and the
degree of lignification since a strong positive correlation
exists between wood stiffness and the percent volume
fraction of axial tissues and the extent to which cell walls
are lignified in P. pringlei. Even though no strong cor-
relation exists between wood stiffness and fiber wall
thickness, we draw attention to three facts that suggest
that the correlation should be stronger than is shown by
our results. First, the stiffest wood in this species contains
fibers that, on average, have the thickest cell walls as well
as the highest percent volume fraction of axial tissues.
Second, the correlation between tissue stiffness and the
apoplastic volume fraction becomes statistically significant
when the data from the youngest portion of the vascular
bundles (i.e., segment E) are removed from consider-
ation. And, third, the stiffness measured for tissue sam-
ples with small transverse areas is not representative of
the stiffness of larger tissue samples because samples
with small transverse areas have disproportionately more
damaged cell walls, which reduces their effective stiff-
ness compared to their larger counterparts. Similarly, tis-
sue samples with small cross-sectional areas contain few
cells per unit transverse surface area. This is important
because the stiffness of any tissue sample increases, to a
limit, as the number of adjoining transverse and radial
cell walls increases.
When these three factors are considered collectively,
we believe they point to the conclusion that fiber wall
thickness is more relevant to the stiffness of P. pringlei
wood than is indicated by our statistical analyses. We
note further that the walls of the ray tissues are relatively
thin throughout the length of the vascular bundles. In
summary, we believe that the data affirm that the bulk
stiffness of wood samples drawn from different locations
along the length of the vascular bundles is significantly
correlated with and an emergent mechanical property of
cell wall lignification and the overall apoplastic volume
fraction of the wood, which increases as a function of
both the volume fraction of the axial tissues and fiber
wall thickness.
This conclusion is further supported by the observation
that wood stiffness measured in the radial and tangential
directions are positively correlated with the volume frac-
tion of axial tissues. If the hypothesis that stiffness is a
mechanical correlate of the apoplastic volume fraction is
correct, then we must expect stiffness measured in either
of the orthogonal directions to be correlated with this
anatomical feature. Nonetheless, our data show that wood
stiffness measured in the tangential plane of anatomical
reference is less perfectly correlated with the volume
fraction of axial tissues than is wood stiffness measured
in the radial direction. One possible explanation is that,
in younger tissue samples, the ray and axial tissues are
nearly parallel in their alignment when viewed in the
transverse plane of section, whereas, in progressively old-
er portions of the same vascular bundle, these two wood
components increasingly diverge from a parallel align-
OF BOTANY [Vol. 87
ment and assume an outwardly ‘‘flared’’ configuration as
a result of the tangential (circumferential) expansion of
the vascular cambium. In terms of experimental proce-
dure, this ‘‘flared’’ anatomy makes it increasingly diffi-
cult to align externally applied bending forces in the tan-
gential plane of sections through wood samples during
bending experiments, and thus has the potential to pro-
duce experimental measurements of wood stiffness that
represent a hybrid between the stiffness measured in the
radial and tangential directions. In contrast, the transverse
shape of even the oldest portion of a vascular bundle
makes it easier to align bending forces in a near or pure
radial direction, thereby making the determination of the
radial stiffness of wood samples less ambiguous. Under
any circumstances, stiffness measured in the radial and
tangential directions correlates well with the volume frac-
tion of axial tissues in wood samples, regardless of where
they are drawn from along the length of vascular bundles,
which lends credence to the hypothesis that the apoplastic
volume fraction and the degree to which it is lignified
have an overriding influence on wood stiffness.
Stem biomechanics—We conclude that the stiffness of
P. pringlei vascular strands correlates significantly with
the apoplastic volume fraction and lignin content of the
wood and that these features vary along the length of
individual growth layers and from one wood growth layer
to another in individual vascular strands. Since they
evince a high degree of repeatable spatial (and, presum-
ably, temporal) ordering and have now been reported for
three representative stems of this species, these variations
in wood stiffness cannot be reasonably ascribed to tissue
fatigue brought about by chronic stem flexure or disease,
but rather lend support to the plausibility that regulatory
factors affecting the vascular cambium and its derivatives
are sensitive and responsive to the force gradients estab-
lished by stem self-loading and externally applied loads.
In the absence of direct experimental manipulation of
stem development, this hypothesis can be inductively ex-
plored, first, by establishing the nature of the force and
stress gradients existing in the columnar stems of P. prin-
glei based on engineering first principles, and, second, by
determining whether the variations in wood anatomy and
stiffness observed in stems correlate with these gradients
in a manner that suggests developmental modifications
occur and are functionally adaptive. The nature of the
force and stress gradients experienced by P. pringlei
stems follows directly from engineering first principles.
Any vertical support member must support its own
weight (self-loading) and the lateral loads exerted on it
by drag forces (wind-loads) (Timoshenko and Gere,
1961; Wainwright et al., 1976; Vogel, 1981; Niklas,
1992). Both of these loading regimes are easily evaluated
in the biological context of the comparatively simple
morphology of P. pringlei stems. Because these stems
are massive in girth relative to their height, they have a
large axial second moment of area everywhere along
their length. Calculations show that this ‘‘geometric con-
tribution’’ to the ability to resist bending is more than
sufficient to cope with the weight of the stem. However,
this ability is augmented significantly by the longitudinal
variations in the cross-sectional area and the stiffness of
the vascular strands. The basipetal increase in the com-
April 2000] NIKLAS ET AL.—CACTUS WOOD BIOMECHANICS
bined cross-sectional area of all the vascular strands and
the nonlinear, complex variation in their stiffness produce
a steady basipetal increase in axial (self-loading) stresses.
In the absence of the observed pattern in wood stiffness,
calculations show that self-loading stresses would reach
maximum intensity near or just below the stem’s midspan
(i.e., in segments B or C; see Fig. 10A). Such a ‘‘stress-
rise’’ could result in the compressive failure of thin-
walled tissues, since the magnitudes of the stresses that
would result in the absence of the less stiff wood in seg-
ment A exceed the compressive yield stress of parenchy-
ma. Thus, in terms of self-loading, there is a clear me-
chanical benefit conferred by the production of less stiff
wood in segment A.
The less stiff wood in segment A may also be bene-
ficial in terms of wind-loading. A large wind-induced
bending moment has the potential to uproot a massive
stem in the absence of a strong anchoring root system.
Based on the specific dimensions of the P. pringlei stem
examined here, the location of the less stiff wood in seg-
ment A corresponds to where the magnitude of any wind-
induced bending moment reaches near maximum inten-
sity and where the rate of change of any wind-induced
bending moment decreases significantly (see Fig. 11A).
These observations afford a plausible biomechanical
explanation for the formation of less stiff wood in vas-
cular strands (in the distal portions of segment A) just
above the region in the stem where continuous growth
layers of wood establish a solid core of wood (in the
proximal portions of segment A). This explanation as-
sumes that the basipetal increase in the cross-sectional
area of the vascular stands contributes to the mechanical
stability of a self-loaded stem. Under these circumstanc-
es, the presence of less stiff and more flexible wood at
the location where the rate of change of bending mo-
ments is low (and where bending moments and stresses
nearly reach their maximum intensity) permits a massive
P. pringlei stem to elastically flex yet simultaneously pre-
serves the interface of adjoining tissues differing in ma-
terial properties to remain intact and thus avoid failure in
shearing (Fig. 12). Although even substantial elastic stem
flexure does not significantly reduce the wind-induced
bending stresses or moments (e.g., 168 stem-tilt would
reduce the bending stresses by ,10% and the bending
moment by ,2%), any column will bend to some degree
in the wind and thus experience bending shear stresses.
Although the vascular strands of P. pringlei are located
away from where shear stress are maximized in any cross
section, failure in shear is still likely to occur wherever
strain-compatibility is lost (i.e., at the interface between
any two materials manifesting different strains when sub-
jected to the same stress). Normally, wood tends to be
the stiffest and least extensible plant tissue known,
whereas primary tissues, such as parenchyma, are the
least stiff and the most extensible. Acknowledging that
the wood of P. pringlei is arranged in a sympodial vas-
cular system and that the vascular strands examined in
our study are laterally interconnected and not technically
‘‘independent’’ structural elements, we point out that the
lateral interconnecting strands of the sympodia are slen-
der and weak in all but the oldest portions of stems and
thus do not provide an effective system of ‘‘lateral
struts.’’ Unlike other woody arborescent species, which
479
Fig. 12. Biomechanical model for a self- and wind-loaded P. prin-
glei stem (left and right longitudinal cutaways, respectively) in relation
to the flexural rigidity EI and stiffness E measured at five locations (A–
E) along the lengths of its vascular strands (graphs). In the absence of
high lateral wind speeds, the stem can maintain its vertical growth pos-
ture and self-loading in part by the virtue of the exponential increase
in the EI of vascular strands toward the base of stem. However, when
subjected to lateral wind speeds incurring high drag forces, the vertical
stem will elastically bend downwind and its tissues will experience
compressive and tensile bending stresses (s2 and s1, respectively),
and shear stresses t will develop at the interface between adjoining
tissues differing in their bulk material properties (see insert). Shear
stresses will reach their maximum intensities near the base of the stem
above the region where vascular bundles become fused together due to
the accumulation of secondary xylem because this portion of the stem
acts as a mechanical pivot point. The low stiffness E and comparatively
high extensibility 1/E of wood produced in the region of the pivot point
(segment A) permits large shear strains and thus reduces the likelihood
of the rupture of cells interfacing with the wood.
establish continuous growth layers of wood and thus an
internal solid core of wood throughout much of the length
of their woody stems, the woody vascular strands of P.
pringlei stems are thus more or less mechanically inde-
pendent of one another along much of the length of the
stem. They join together only near the base of the stem
where they form a solid mass of wood that serves as a
rigid and inflexible foundation to the stem. Since the
woody vascular strands of P. pringlei are free along much
of their length in the stem and theoretically can fail in
shearing at their interface with nonwoody tissues or un-
differentiated cells, we surmise that the structural integ-
rity of the vascular strands is preserved when stems are
wind-loaded by the presence of an elastically extensible
‘‘joint’’ at their base just above the woody core at the
stem foundation. This ‘‘joint’’ is composed of less stiff
and more extensible wood and thus can elastically deform
and preserve its contact with adjoining cells and tissues
(Fig. 12).
The location of this joint just above the woody stem
foundation is more or less ideal because it reduces the
strains experienced by the stem foundation, which is at-
tached to a mechanically ineffective root system. Our
field observations indicate that the root systems of plants
480 AMERICAN JOURNAL
the size studied here are laterally extensive, yet shallow
and weak when placed in tension or compression. As
such, the root system of comparatively young plants may
provide little in the way of mechanical support (except
perhaps immediately near its junction with the stem) and
would serve as a ground-level pivot point in the absence
of a more distal and flexible ‘‘joint’’ along the length of
the stem. Older, more massive plants may increasingly
depend on their root systems for anchorage, such that the
flexible joint may become less useful over time.
The mechanical stability of P. pringlei stems is fos-
tered by their determinate growth in height and the ability
to establish longitudinal and radial gradients in wood
stiffness. Much like the stems of the saguaro cactus (Nik-
las and Buchmann, 1994), those of P. pringlei grow in
height at a steadily decreasing rate and thus essentially
stop growing in height after they achieve a certain size.
In theory, this affords a developmental mechanism that
can assure a suitable factor of safety against mechanical
failure provided that mature stem size and anatomy are
developmentally prefigured (Niklas, 1992, 1994; Niklas
and Buchmann, 1994). Our data clearly indicate that the
P. pringlei vascular cambium and the pattern of matu-
ration in its derivatives can produce wood in a single
growth layer that differs in stiffness along the length of
the stem. The bulk stiffness of a vascular strand at any
particular location along its length can also be adjusted
by adding less or more stiff wood (see Fig. 5). Since the
relative difference in the stiffness of wood added in each
growth layer can be conserved as a stem increases in
height, longitudinal gradients in P. pringlei wood stiff-
ness can be established in the juvenile condition and
maintained as a stem grows to reach its final height. Like-
wise, since stiffer wood can be added at each location
along the length of a growth layer as a stem grows, the
bulk stiffness of the vascular strands can be modified over
time to mechanically accommodate increases in stem
weight and height. Thus, P. pringlei stem development
has the ability to prefigure longitudinal gradients in the
material properties of its woody vascular stands as
growth proceeds, yet preserves the capacity to adjust the
absolute magnitudes of these properties as the stem in-
creases in weight and height.
This phenomenology, which is described here for the
first time, plays an important role in the optimization of
a number of anatomical and morphological features,
some of which are less conducive to mechanical stability
than others. The stems of P. pringlei function well me-
chanically but clearly within the constraints imposed on
them by their manifold functional obligations and their
apparently specialized growth and development. More-
over, optimization should be viewed in a broader context.
Our biomechanical analyses demonstrate that mechanical
stability in terms of self-loading and wind-induced stem
flexure is fostered by the production of a disproportion-
ately large volume fraction of ray tissues and a reduction
in the lignin content of secondary vascular tissues near
the base of P. pringlei stems. However, because these
advantages are a consequence of a variety of wood ana-
tomical features that are developmentally correlated and
that undoubtedly affect many biological functions, they
cannot be judged to be a consequence of natural selection
operating directly or exclusively on mechanical stability,
OF BOTANY [Vol. 87
although it is clear that selection acting on one aspect of
wood anatomy will have consequences on other corre-
lated anatomical features. In this regard, we note that
among 77 surveyed P. pringlei plants, lateral branches
generally emerge ;1 m from the base of the central stem,
and that the number of branches increases as plants age.
Therefore, the reduction in wood stiffness in this vicinity
correlates with general plant morphology. Preliminary
observations reveal that the widest rays accommodate
vascular traces. The preponderance of wide rays in a sam-
ple reduces the value obtained for % axial tissue. Further
investigations may reveal that the support of lateral
branches is facilitated by a superabundance of large rays
in the region of reduced vascular stiffness.
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APPENDIX
A ‘‘transformed-section’’ method was used to compute the stresses
that occur as a result of the self-loading of the P. pringlei stem, which
was modeled as a support member (column) composed of two materials,
one of which is more stiff and another (i.e., woody vascular strands and
surrounding tissues). This approach was taken because it is necessary
to compensate for the effect of the stiffer material on the stress expe-
rienced by the less stiff material(s) by enlarging the cross-sectional area
of the stem until it is equivalent to that of a stem composed exclusively
of the least stiff material.
The transformed-sectional area AT for any column composed of two
materials differing in stiffness was derived by first noting that the stress
si resulting from any axial load Pi acting on any cross-sectional area Ai
is given by the formula si 5 Pi/Ai which, in turn, equals the product of
the resulting strain «i and a Young’s modulus Ei (i.e., si 5 «iEi). Thus,
the transverse area of a column composed of the less stiff material is
given by the formula
1 PT
AT 5 , necessarily increase basipetally, provided that the term (Es /Ec 2 1)As
ec Ec
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481
where PT is the total axial load acting on any cross section, and «c and
Ec are the strain and the Young’s modulus of the less stiff material,
respectively. Since PT equals the loads supported by the stiff and less
stiff materials in the columnar stem (i.e., PT 5 Ps 1 Pc), the trans-
formed-sectional area is given by the formula
(Ps 1 Pc )
AT 5 .
ec Ec
Since Pi 5 «iEiAi holds generally, it follows mathematically that
(es Es As 1 ec Ec Ac )
AT 5 ,
ec Ec
where «s and Es are the strain and the Young’s modulus of the stiffer
of the two materials in the columnar stem, respectively. Since both
materials in the stem must have equivalent strains « (i.e., «s 5 «c 5 «i)
to accord with the theory of elastic stability, we see that
Es
AT 5 As 1 Ac ,
Ec
and, since the cross-sectional area Ai anywhere along the length of the
stem equals As 1 Ac, the transformed-sectional area is thus given by the
formula
1E 2 12 A .
Es
AT 5 Ai 1 s
c
Note that this formula, which reduces to Ai when the two materials
have equivalent Young’s moduli, is a ‘‘weighted’’ cross-sectional area,
that is, the term (Es /Ec 2 1)As expresses the volume fraction of the
stem’s stiffest material (wood) in terms of its material stiffness relative
to that of the less stiff material. Since the effective (compressive) stress
experienced by both materials in the stem equals PT /AT, this stress is
reduced as either Es or As (or both) increases (i.e., stress is reduced by
either increasing the stiffness of the wood or by increasing the amount
of wood in the cross section). Noting that PT increases basipetally from
the top to the bottom of any vertical stem and that, for any cross section
Ai, PT 5 S (r·g·Ai·,i), where r is the bulk density of all stem tissues
and ,i is distance from the top of the stem, the effective stress does not
varies nonlinearly along stem length.