Tree Physiology 20, 535–540
© 2000 Heron Publishing—Victoria, Canada
Thigmomorphogenesis: changes in the morphology and mechanical
properties of two Populus hybrids in response to mechanical
perturbation
MICHELE L. PRUYN,1 BENJAMIN J. EWERS, III2 and FRANK W. TELEWSKI3
1
Department of Forest Products and Department of Forest Science, Forest Research Laboratory, Richardson Hall, Oregon State University,
Corvallis, OR 97331-7402, USA
2
Orthopaedic Biomechanics Laboratories, College of Osteopathic Medicine, Michigan State University, East Lansing, MI 48824, USA
3
Department of Botany and Plant Pathology, W.J. Beal Botanical Garden, Michigan State University, East Lansing, MI 48824, USA
Received January 30, 1998
Summary To identify hybrid-specific differences in developmental response to mechanical perturbation (MP), we compared the effects of stem flexure on several morphological and
mechanical properties of two Populus trichocarpa Torr. &
A. Gray × P. deltoides Bartr. ex Marsh. hybrids, 47-174 and
11-11. In response to the MP treatment, both hybrids exhibited
a significant increase in radial growth, especially in the direction of the MP (47-174, P = 0.0001; 11-11, P = 0.002), and a
significant decrease in height to diameter growth ratio (P =
0.0001 for both hybrids), suggesting that MP-treated stems are
more tapered than control stems. A direct consequence of the
MP-induced increase in radial growth was a significant increase in flexural rigidity (EI, N mm 2) in stems of both hybrids
(47-174, P = 0.0001; 11-11, P = 0.009).
Both control and MP-treated stems of Hybrid 47-174 had
significantly greater height to diameter ratios and EI values
than the corresponding stems of Hybrid 11-11 (11-11 stem ratios and EI values were 85 and 76%, respectively, of those of
47-174). In Hybrid 47-174, Young’s modulus of elasticity
(E, N mm –2), a measure of stem flexibility, for MP-treated
stems was only 80% of the control value (P = 0.0034),
whereas MP had no significant effect on E of stems of Hybrid
11-11 (P = 0.2720). Differences in flexure response between
the hybrids suggest that Hybrid 47-174 can produce a stem
that is more tolerant of wind-induced flexure by altering both
stem allometry and material properties, whereas Hybrid 11-11
relies solely on changes in stem allometry for enhanced stability under MP conditions.
Keywords: developmental acclimation, flexural rigidity, plantation forestry, second moment of cross-sectional area, wind
tolerance, Young’s modulus of elasticity.
Introduction
Wind stress can greatly impact the productivity and survival of
a forest stand (Grace 1977). Jaffe (1973, 1980) used the term
“thigmomorphogenesis” to describe the physiological, bio-
chemical and morphological responses of plants to wind and
other mechanical perturbations. Thigmomorphogenesis can
prevent stem failure caused by wind loading, by reducing drag
or increasing mechanical strength, or both (Telewski and Jaffe
1986a, 1986b, Telewski 1995). In field experiments, all possible plant responses to wind can occur simultaneously, making
it difficult to isolate their individual effects on plant growth
(Biddington 1986). The wind-induced, back and forth motion
of plants has been generated artificially under controlled laboratory conditions by mechanically perturbing stems (Mitchell
et al. 1975, Jaffe 1976, Biro et al. 1980, Biddington and Dearman 1985). Such treatments, referred to as mechanical perturbation (MP), can reveal effects of wind-sway on plant growth
habit and physiology.
Plant responses to wind have been characterized extensively in gymnosperms, and to a lesser extent in woody angiosperms. In gymnosperms, morphological responses to MP
include formation of an elliptically shaped stem cross section,
with the long axis in the direction of flexure, and decreased
stem height (Jacobs 1954, Larson 1965, Telewski and Jaffe
1986a, 1986b). Similar morphological responses occur in the
woody angiosperms Liquidambar styraciflua L. (Neel and
Harris 1971) and Ulmus americana L. (Telewski and Pruyn
1998). Mechanical responses to MP in the gymnosperms,
Pinus taeda L. and Abies fraseri (Pursh) Poir., include increased flexural rigidity (EI) or a stronger stem, and decreased
Young’s modulus of elasticity (E) or a more flexible stem
(Telewski and Jaffe 1986a, 1986b). There have been few studies of mechanical responses to MP in woody angiosperms;
however, Holbrook and Putz (1989) noted that whole-tree
flexibility of free-swaying Liquidambar styraciflua stems was
not significantly different from that of constrained stems.
Based on variation in morphological characteristics associated with wind toppling among a group of Populus hybrids,
Harrington and DeBell (1996) identified Hybrid 47-174 as the
most resistant to wind toppling or leaning and Hybrid 11-11 as
the most susceptible. Thus, compared with Hybrid 11-11, Hy-
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PRUYN, EWERS AND TELEWSKI
brid 47-174 was characterized by a greater degree of lower
stem taper, less aboveground biomass per unit of cross-sectional root area, and larger roots. We have extended this study
to characterize several mechanical responses to MP in stems
of two P. trichocarpa Torr. & A. Gray × P. deltoides Bartr. ex
Marsh hybrids, 47-174 and 11-11. We tested the hypothesis
that hybrid-specific traits of Populus dictate hybrid response
to mechanical stress. We also tested the notion that the two hybrids can serve as a model system for poplar forestry management practices that are strongly affected by individual tree and
forest stand susceptibility to wind damage.
Materials and methods
Culture of the plants
Stem cuttings, which were drawn from the populations of
47-174 and 11-11 hybrids used by Harrington and DeBell
(1996), were obtained from Washington State University’s
Farm Five, Puyallup, WA and rooted in a nursery at Michigan
State University (MSU). The rooted cuttings were transplanted to 7.3 × 7.3 × 22.8 cm pots (Anderson Die and Manufacturing Company, Portland, OR) containing a 1:1 (v/v) mix
of high porosity soil (Baccto, Michigan Peat Company, Houston, TX) and a recycled, sterilized sandy soil (MSU greenhouse). The cuttings were cultivated in a greenhouse in a
12–14 h photoperiod at 25 °C. After sprouting, the cuttings
were transplanted twice, first to 8-liter pots and then to 18-liter
pots. The original stem cuttings were left to grow undisturbed
for 2 weeks after final transplanting. During this time, new
shoots elongated on each stem cutting. At the end of two
weeks, a leader stem was selected from each cutting for uniform height and stem width and then staked. Any other lateral
shoots on the original stem cutting were removed.
Eighteen individuals per hybrid were selected and nine individuals per hybrid were randomly assigned to each treatment.
The two treatments were control and mechanical perturbation
(MP), which consisted of 20 flexures (back and forth) in the
NE to SW direction to each stem. Six rows of three plants per
row were arranged on two rectangular benches with each row
alternating between control and MP. The hybrids were restricted to separate benches, which presents the possibility of a
confounding variable in terms of hybrid effect; however, we
believe this effect was minimal because of the uniformity of
the greenhouse environment.
The flexure treatments were administered once daily during
July and August 1996. Before treatments began, a point of
flexure was chosen for the stems just above the fourth node
from the base of each leader stem. For each daily treatment,
the stem was grasped at the flexure point with the thumb and
forefinger. With the other hand, the stem was grasped several
centimeters above the flexure point and bent back and forth, at
an angle of 30–45° from the original vertical position of the
stem. After treatment, the stem was returned to the vertical position and re-staked. Staking has been known to reduce MP responses in trees (Jacobs 1954, Holbrook and Putz 1989);
however, staking was necessary in this experiment because the
Populus stems could not support themselves after reaching
approximately 15 cm in length. Stems left to lean without support showed gravitropic responses, making it impossible to
isolate responses solely caused by MP.
Plants were fertilized once after 1 month of treatment with a
commercial 20,20,20 N,P,K fertilizer (30 g per 4 l). During the
experiment, pesticides were applied three times to control
aphids and white fly.
Morphological measurements
Before and after the 2-month treatment, shoot heights (cm)
and diameters (mm) at the point of flexure were recorded.
Stem diameter was measured with a digital caliper in the direction of flexure (NE to SW; MPpar axis) and in the direction
perpendicular to flexure (MPperp axis). Ratios of stem height
growth to diameter growth on the MPpar axis were calculated.
Ratios of stem diameter growth on the MPpar axis to stem diameter growth on the MPperp axis were calculated to determine
an index of stem roundness. For the control stems, the measured axes corresponded to those of the MP-treated stems. The
ratio means were tested against the null hypothesis that the
stems are round (i.e., have a ratio of 1.0).
Mechanical properties
After the final measurements were recorded, a 14-cm section
was cut from each stem having the point of flexure at its center. Maximum and minimum diameters of the stem sections
were recorded at three points. The mean radius (r) was calculated for each stem from the diameter measurements and used
to calculate second moment of cross-sectional area (I, mm 4).
Flexural rigidity (EI, N mm 2), a function of modulus of
elasticity (E, N mm –2) and I, was determined for each specimen by the four-point bending test (Wainwright et al. 1976)
(Figure 1). This test was conducted at room temperature
(~20 °C) by deflecting the stems with an Instron, Model 1331,
retrofitted with 8500 electronics by the Biomechanics Department, MSU. To calculate EI, we used the equation given by
Gere and Timoshenko (1990):
EI = ( F / V )( a 2 / 12)( 3 L − 4 a ).
(1)
Each stem was bent on a tangential plane with simple beams
supporting each end of the stem. The distance between the two
supported ends was 70 mm, and is referred to as the span
length (L) (Figure 1). The stem was displaced at two points
along L at 0.5 mm s –1, while a load cell recorded the resulting
load. This displacement continued until a load of 45.6 kg was
reached. The distance between one supported end and the
nearest load (F), designated a, was equal to 20.0 mm on each
end of the stem (Figure 1). The slope of the linear portion of
the curve load (F) versus distance deflected (V) was calculated. Values of F/V, L, and a were used in Equation 1 to calculate EI. We used the equation of Gere and Timoshenko (1990)
to calculate I:
I = πr 4 / 4.
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RESPONSE OF POPULUS TO MECHANICAL PERTURBATION
Figure 1. Diagrammatic representation of a stem segment loaded on
an Instron for a four-point bending test. The stem is shown before
(solid line) and after loading (broken line). As the load (F) is exerted
on the stem, the Instron measures the stem’s displacement (V) as
strain. Abbreviations: L is span length, and a is distance between F
and the stem support at either end. Adapted from Gere and
Timoshenko (1990).
Young’s modulus of elasticity (E; N mm –2) was calculated by
dividing EI by I.
Statistical analyses
Data are presented as a mean and standard error for each treatment. All responses of the populations (except the roundness
index) were tested for significant differences by a two-way
analysis of variance (2-way ANOVA) with factors of hybrid
(47-174, 11-11), flexure treatment (control, MP), and their interaction. The data met the assumptions of the ANOVA;
namely, the residuals fit a normal distribution and had constant variance. Least Squares Means (LSMEANS) and the respective standard errors were computed for the response
variables. The LSMEANS are averages of the expected values
over the factors of hybrid and treatment in the model. The
standard errors were calculated for main effects of hybrid and
treatment (n = 18), and for the interaction effect of hybrid by
treatment (n = 9). Pair-wise comparisons (t-tests) between
specific means were made with Fisher’s Protected Least Significant Difference (FPLSD) procedure (Fisher 1966).
Stem roundness was tested by subtracting 1.0 from each
MPpar/MPperp ratio, assuming that a round stem would have a
ratio of 1.0. The differences were then analyzed by univariate
analysis, which computed a t-test against the null hypothesis
that the differences were equal to zero. All P-values are presented as the probability (Pr) that the absolute value of the
means (|T|) are greater than zero. All statistical procedures
were conducted with Statistical Analysis Systems software,
release 6.12 (1996; SAS Institute Inc., Cary, NC).
Results
Morphological properties
In both hybrids, the MP treatment significantly increased stem
diameter growth along both the MPpar and MPperp axes (Table 1). Although there was no difference in control stem diameter growth between Hybrids 47-174 and 11-11, diameter
growth of flexed 47-174 stems was greater than that of flexed
537
11-11 stems (P = 0.0325) (Figure 2a). However, there was no
evidence of an interaction between hybrid and treatment for
either axis (Table 1). The roundness index ((MPpar /MPperp)
– 1.0) for MP-treated stems of both hybrids differed significantly from zero, whereas it was not significantly different
from zero in the control stems (Table 1). Stem diameter
growth on the MPpar axis was greater than that on the MPperp
axis in all MP-treated stems, indicating that the stems were elliptical in the direction of flexure (Table 1).
Height growth of flexed 47-174 stems was greater than that
of flexed 11-11 stems (P = 0.0325) (Figure 2b), because the
MP treatment inhibited stem height growth of Hybrid 11-11,
whereas it increased stem height growth of Hybrid 47-174
(Table 1). The height to diameter growth ratio was higher in
Hybrid 47-174 than in Hybrid 11-11 (P = 0.0007), and lower
in MP-treated stems than in control stems (P = 0.0001) (Figure 2c). There was no evidence of a hybrid-by-treatment interaction on the height to diameter growth ratio (Table 1).
Mechanical properties
There were significant effects of hybrid and MP treatment on
stem flexural rigidity (EI). Thus, Hybrid 47-174 had higher EI
values than Hybrid 11-11 (P = 0.0008) (Table 1) and MPtreated stems had higher EI values than control stems (P =
0.0001) (Figure 3c). This finding indicates that the trend of increased I in response to mechanical flexure more than compensated for the MP-induced decrease in E (Figure 3). The
trends illustrated in Figure 3a suggest that the increase in I in
MP-treated stems was greater in Hybrid 47-174 than in Hybrid
11-11. Control stems of Hybrid 47-174 also had higher I values than control stems of Hybrid 11-11, resulting in higher EI
values.
The MP treatment decreased the stem’s modulus of elasticity, (E, N mm –2) (P = 0.0048), indicating that MP-treated
stems were more flexible than control stems. The MP-induced
decrease in E was significant in Hybrid 47-174, but not in
Hybrid 11-11 (Table 1). There was no difference in E between
control stems of Hybrids 47-174 and 11-11 (Figure 3b) and
there was no evidence of a hybrid-by-treatment interaction on
E (Table 1).
Discussion
We observed both morphological and mechanical responses to
flexure stress in two Populus hybrids. Morphological responses of MP-treated stems included the development of an
elliptical stem cross section at the flexure point (roundness index, Table 1), and a 70% decrease in height to diameter
growth ratio (height/MPpar axis; Figure 2c), compared with
control values. Mechanical responses of MP-treated stems included a 31% increase in flexural rigidity (EI) (Figure 3b) and
a 14% decrease in Young’s modulus of elasticity (E) (Figure
3c), compared with control values.
McMahon (1973) described a tree as a self-supporting column under loading conditions. This concept can be used to explain the observed responses to mechanical perturbation.
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PRUYN, EWERS AND TELEWSKI
Table 1. Morphological and mechanical responses in stems of Populus Hybrids 47-174 and 11-11 to mechanical stress. Hybrid P-values are from
pair-wise comparisons among means based on FPLSD. Hybrid-by-treatment interaction P-values are listed for each variable. Deviation of the
roundness index from zero was evaluated by a t-test (probability, Pr > absolute value of mean, |T|).
Property
Hybrid 11-11
Control
Morphological properties
Stem diameter growth, MPpar axis (mm)
Stem diameter growth, MPperp axis (mm)
Roundness index (MPpar /MPperp – 1)
Pr > |T|
Stem height growth (cm)
Stem height to MPpar growth ratio
Hybrid 47-174
MP
P-value Control
3.32 ± 0.18
4.17 ± 0.18
3.35 ± 0.17
4.03 ± 0.17
–0.007 ± 0.21 0.036 ± 0.21
0.2891
0.0002
83.3 ± 3.61
77.6 ± 3.61
25.5 ± 1.01
18.6 ± 1.01
Mechanical properties
Flexural rigidity × 105 (EI; N mm 2)
Second moment of cross-sectional area (I; mm 4)
Young’s modulus of elasticity × 103 (E; N mm –2)
1.98 ± 0.20
81.5 ± 12.4
2.51 ± 0.11
MP
0.002
3.34 ± 0.18 4.74 ± 0.18
0.008
3.24 ± 0.17 4.51 ± 0.17
–
–0.032 ± 0.21 0.053 ± 0.21
–
0.4454
0.0005
–
94.6 ± 3.61 104.4 ± 3.61
0.0001
29.7 ± 1.01 22.1 ± 1.01
2.76 ± 0.20 0.009
121.8 ± 12.4 –
2.33 ± 0.11 0.2720
Figure 2. Effects of mechanical perturbation on height and diameter
growth of Populus shoots. Values are means ± SE; n = 9. (a) Effects of
hybrid and mechanical perturbation on stem diameter growth on the
MPpar axis (P = 0.1795 and 0.0001, respectively). (b) Effect of hybrid-by-treatment interaction on stem height growth (P = 0.039). (c)
Effects of hybrid and mechanical perturbation on the ratio of height to
diameter (MPpar axis) growth (P = 0.0007 and 0.0001, respectively).
Interaction
P-value P-value
0.0001
0.0001
–
–
–
0.0001
0.083
0.162
–
–
0.039
0.742
2.46 ± 0.20 3.76 ± 0.20 0.0001 0.211
99.0 ± 12.4 191.6 ± 12.4 –
0.043
2.52 ± 0.11 2.02 ± 0.11 0.0034 0.158
Telewski and Jaffe (1986a, 1986b) concluded that many of the
observed responses in wind-stressed or mechanically perturbed trees are examples of developmental acclimation, enabling the trees to withstand bending and swaying stresses better
by reducing drag and increasing mechanical strength. These
conclusions are supported by the constant-strain hypothesis
for developing wood in tree stems, described by Wilson and
Archer (1979). According to the constant-strain hypothesis,
the distribution of new wood is regulated by the degree of
strain in various regions along the stem (Mattheck 1991). Developing trees tend to conform to a shape that stabilizes the
maximum strains along a stem. The morphological responses
to MP observed in this study (elliptical stem formation and reduced growth ratios) reflect this directed allocation of wood.
The observed responses in stem mechanical properties to
flexure support the hypothesis that stems develop to stabilize
maximum strains according to their hybrid-specific traits.
Thus, MP-treated stems of Hybrid 47-174 had higher second
moment of cross-sectional area (I) values than MP-treated
stems of Hybrid 11-11 (Figure 3b), leading to more rigid
stems. Flexural rigidity (EI, N mm 2) in MP-treated stems of
Hybrid 11-11 was only 84% of that in MP-treated stems of
Hybrid 47-174 (Figure 3c). The second moment of cross-sectional area (I) adds a structural component to EI because it
represents the position of the central weight within a stem’s
cross-section, thus describing the overall strength and stability
of stem architecture. Young’s modulus of elasticity (E,
N mm –2) describes the flexibility of the tissue constituting the
stem. The MP-induced increase in (I) overrode the effect of
the MP-induced decrease in E, because I is scaled to the fourth
power of stem radius. Hence, the flexure-directed elliptical
shape of MP-treated stems is largely responsible for their increased rigidity.
Although increased flexibility resulting from the MP-induced decrease in E was obscured by the MP-induced increase
in I, it is important to consider trends in E to understand the
stem’s mechanical capabilities. The MP-induced decrease in
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RESPONSE OF POPULUS TO MECHANICAL PERTURBATION
539
Hybrid 11-11 lacked wind resistance, is in agreement with observations of Harrington and DeBell (1996). The height to diameter growth ratio (height/MPpar axis, Figure 2) and EI
(Figure 3) of Hybrid 47-174 were 17 and 31% higher, respectively than those of Hybrid 11-11. Telewski and Jaffe (1981,
1986a, 1986b) suggested that the reduction of growth rate of
the crown would reduce the surface area available to resist the
wind, resulting in less drag. Hybrid 11-11 responded to MP by
reducing its stature to avoid wind drag, whereas Hybrid 47174 enhanced its resistance to wind by increasing stem rigidity.
In conclusion, Populus Hybrids 47-174 and 11-11 differ in
their morphology (height growth) and mechanical properties
(I) that directly affect tolerance of mechanical perturbation.
Anatomical and biochemical analyses of stem cross sections
may lead to an explanation of the observed changes in the material and structural properties of the wood of flexed stem of
Hybrid 47-174 at the cellular level.
Acknowledgments
Figure 3. Effects of mechanical perturbation on mechanical properties of Populus stems. Values are means ± SE; n = 9. (a) Effects of hybrid and mechanical perturbation on flexural rigidity (EI, N mm 2) (P
= 0.0009 and 0.0001, respectively). (b) Effect of hybrid-by-treatment
interaction on second moment of cross-sectional area (I, mm 4) (P =
0.0429). (c) Effects of hybrid and mechanical perturbation on modulus of elasticity (E, N mm –2) (P = 0.2172 and 0.0054, respectively).
E in stems of Hybrid 47-174 (Figure 2b) is similar to the response observed in flexed stems of Abies fraseri and Pinus
taeda (Telewski and Jaffe 1986a, 1986b). Wilson and Archer
(1979) suggest that changes in E during stem development reflect changes in the type of wood being formed. Decreased E
in MP-treated stems of Hybrid 47-174 MP may be the result of
the formation of wood types that have increased ability to absorb bending energy under the force of MP, thereby enhancing
resistance of the stems to failure from wind stress. In contrast,
the MP treatment did not significantly affect E in Hybrid
11-11 stems (Table 1). In Liquidambar styraciflua, stem allometry accounted for most of the observed differences in tree
stability (Holbrook and Putz 1989). Similarly, the non-significant decrease in E of MP-treated stems of Hybrid 11-11 suggests that these stems also relied predominantly on changes in
stem allometry (e.g., radial growth, growth ratio, and I (Table
1)) for enhanced stability.
Our finding that Hybrid 47-174 was wind resistant, whereas
The authors thank Dr. H.D. Bradshaw, Jr. and Dr. R.F. Stettler, University of Washington for providing the hybrid poplar cuttings grown
at Washington State University’s Farm Five in Puyallup, WA, and Dr.
C.A. Harrington, USDA Forest Service for valuable discussion.
Thanks also to T. Boland, Beaumont Nursery, Grounds Maintenance
Department, Michigan State University, for providing assistance in
the propagation of the Populus stem cuttings; and D. Freeville and
M. Olrich, Botany and Plant Pathology Department greenhouses,
Michigan State University, for executing pesticide application and
greenhouse maintenance. Also, thanks to P. Atkinson and Dr. R.
Haut, Biomechanics Department, Michigan State University, for their
assistance in the use of the Model 1331 Instron.
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