Tree Physiology 26, 73–79
© 2005 Heron Publishing—Victoria, Canada
Righting response of artificially inclined maritime pine (Pinus pinaster)
saplings to wind loading
STEPHANE BERTHIER1,2 and ALEXIA STOKES1,3
1
Laboratoire de Rhéologie du Bois de Bordeaux, Mixed Unit: INRA/CNRS/Université Bordeaux I, Domaine de l’Hermitage, 69, rte d’Arcachon,
33612 Cestas Cedex, France
2
Current address: Forest Research, Northern Research Station, Roslin, Midlothian, EH25 9SY, U.K.
3
Corresponding author ([email protected])
Received February 14, 2005; accepted May 3, 2005; published online October 3, 2005
Summary To determine if trees respond to dynamic and
static loading in the same manner, 2-year-old maritime pine
(Pinus pinaster Ait.) trees were subjected to different types of
mechanical loading in the field. One block of trees (the control)
were kept in pots and planted in the field at an angle of 0 or 45°
to the vertical. A similar block of leaning potted trees was
planted nearby and subjected to frequent, unilateral wind loading for a period of 1 s every 2 min. Half the leaning trees were
oriented toward the direction of wind loading and half were oriented along the axis of wind loading. The stem profile was
measured three times during the growing season to quantify the
rate of stem straightening. Compression wood formation and
stem shape were measured in all plants.
No differences in mean height or diameter were observed
between blocks and all leaning trees straightened, but not at
the same rate. Although no difference in the rate of apical
straightening occurred between control and wind-treated
trees, the righting response of the basal part of the stem of
leaning trees subjected to wind was four times greater than that
of leaning trees without wind. No differences in the righting
response were observed between leaning trees growing toward
and trees growing away from the source of wind. No significant differences in compression wood formation were found
between control trees and wind-treated trees, indicating that
other factors must determine the reorientation rate of leaning
trees. Results are discussed with reference to the quality of
compression wood in conifers and the mechanotransductive
pathway in plants.
Keywords: compression wood, mechanical stress, stem lean,
thigmomorphogenesis.
Introduction
As early as the 1800s, wind was identified as a significant factor affecting the growth of trees (Metzger 1893), but research
into the mechanism by which plants respond to wind did not
begin until almost 100 years later. The adaptive growth response of plants and trees to mechanical perturbations was
named thigmomorphogenesis by Jaffe (1973); “thigmo” from
the Greek “to touch” and “morphogenesis” implying the changes in form incurred during growth. The first experiments carried out by Jaffe (Jaffe 1973, 1980, Jaffe et al. 1980, Jaffe and
Telewski 1984) investigated the effects of touching, brushing,
rubbing and flexing herbaceous species e.g., bean (Phaseolus
vulgaris L.) and Bryony (Bryonica dioica Jacq.) plants. Typical responses included a reduction in stem elongation and an
increase in radial growth. Later researchers have worked on
trees, notably Telewski (1989, 1990) and Telewski and Jaffe
(1981, 1986a, 1986b), and used flexing machines or wind tunnels to imitate, more realistically, the effects of wind on the
growth of young trees. As a result of mechanical stress, trees
may develop a “stunted” appearance, thus decreasing the
speed-specific drag of the crown. Wind loading is reduced on
the plant itself, especially if the canopy develops a flag-shaped
form, with branches swept to the lee side of the plant (Telewski
and Jaffe 1986a, 1986b, Ennos 1999). Several studies investigated the physiological and hormonal changes in stressed trees
(Telewski and Jaffe 1986c, Telewski 1990), whereas others
studied mechanical damage to plants, e.g., to stomata caused
by the abrasive action of leaves rubbing together in the wind
(Wilson 1984). The first in-depth studies on the effects of wind
action on tree root growth were carried out with Sitka spruce
(Picea sitchensis Bong. Carr) and European larch (Larix decidua Mill.) by Stokes et al. (1995, 1997).
Changes in growth under mechanical loading may also be
observed at the tissue level. In the stem, the number of fibers or
tracheids increases in the direction of flexure, and in the case
of a unidirectional load, e.g., prevailing wind, cell number increases on the leeward side in conifers (Telewski and Jaffe
1981, 1986a, 1986b) and on the windward side in angiosperms
(Timell 1986). This increase in cell number often results in an
asymmetrically shaped stem, which reduces the likelihood of
rupture in the zones under most stress. Telewski (1989) found
that a different type of wood forms in conifers subjected to a
dynamic load, i.e., a small inconsistent load, whereby the tree
returns to the vertical position after the load has been applied,
e.g., light wind gusts. This wood, termed “flexure wood,” has
shorter tracheids than normal wood, increased microfibril an-
74
BERTHIER AND STOKES
gles in the cell wall and a lower longitudinal stiffness. However, all these morphological changes can be found in a more
exaggerated form in conifer stems permanently displaced
from the vertical, e.g., in trees inclined after a storm or heavy
snow fall. Because it appears in zones held in compression,
this wood is called “compression wood” (CW) and is more
dense and lignified, having tracheids with thicker walls and a
rounder cross section than tracheids of normal wood (Timell
1986). As a result of differences in physical and structural
properties of the cell wall, CW serves to straighten the stem
(Archer 1987, Kwon et al. 2001, Fourcaud et al. 2003). Tree
and wood responses to mechanical stress therefore appear to
differ according to whether the loading is static or dynamic,
i.e., responses to a primary dynamic swaying, in which a
gravitropic presentation time (minimum stimulation time required to elicit a response; Telewski 1995) is not achieved, differ from responses to a unilateral displacement of sufficient
duration to induce a gravitropic response (review in Telewski
1995). To our knowledge, the only studies in which tree responses to dynamic and static loading have been compared are
by Larson (1965) and Telewski (1989). Both authors found
that CW forms asymmetrically under uni- or bilateral loading,
but when a multilateral wind force was applied to trees, no CW
was formed.
No study has yet been carried out to examine tree growth
subjected to simultaneous static and dynamic loading, even
though this situation occurs in leaning trees subjected to daily
wind loading. We therefore investigated the effect of dynamic
wind loads on the growth and righting response of leaning
maritime pine (Pinus pinaster Ait.).
Materials and methods
Plant material and growth conditions
Forty-four 2-year-old maritime pines (P. pinaster) trees were
chosen with single, straight stems. Trees were grown in individual 4-l containers, at the forest nursery of INRA Pierroton
(20 km southwest of Bordeaux, France). On May 12, 1999, the
selected population, which had an initial mean stem length (L i )
of 1.01 ± 0.11 m and a mean basal diameter (D i) of 11.9 ±
1.9 mm beneath the bark, was planted in two blocks, 15.0 m
apart, in the nursery. Although the experiment took place in
the field, saplings were kept in containers so as not to disturb
root and shoot growth during transplanting. Trees were watered daily. Mean annual rainfall at Pierroton is 900 mm and
mean annual temperature is 13.5 °C (Cucchi et al. 2004). Natural prevailing wind at a height of 1.5 m was from the northnorthwest during June–September, with mean speeds of
< 0.8 m s – 1.
Block 1, the control plot, included 16 individuals, with a
mean spacing of 1 × 1 m between saplings (Figure 1). These
trees were subjected to the natural environment of the forest
nursery. Trees in Block 2, the treatment plot, which included
the 28 remaining trees, were exposed to artificial wind. Trees
in the wind-treated block were planted 1.15 m apart in a
31.2-m circle. At the center, an 8.0-m-long, horizontal metal
arm rotated continuously once every 2 min. An electrical fan
fixed to one end of the rotating arm exposed saplings to intermittent wind loading (Berthier and Stokes 2005, Tamasi et al.
2005). Saplings were thus exposed to a unilateral airflow with
Figure 1. The experimental
plots. (a) Symbolic representation of a single sapling. In this
case, the sapling is leaning at
45°, with the following digitizing points: A = the apex; B =
the stem base; and R = the
fixed reference point (the top
of a wooden stake in the
ground). (b) The artificial
wind-treated block consisting
of 28 saplings planted in a circle, 10 straight and 18 leaning
at 45°, exposed to wind produced by a revolving fan (F).
Each tree was subjected to artificial wind loading equivalent
to 3.21 m s – 1 for 1 s every
2 min. The prevailing natural
wind direction (WD) was
north-northwest. (c) The control block without artificial
wind, containing six straight
saplings and 10 saplings leaning at 45° in various directions.
TREE PHYSIOLOGY VOLUME 26, 2006
RIGHTING RESPONSE OF WIND-LOADED, LEANING TREES
a mean speed of 3.21 m s – 1 for 1 s every 2 min, both day and
night (Figure 1).
To examine the righting response of leaning conifers with or
without dynamic wind loading, 18 wind-treated trees and
10 controls were inclined at an angle of 45° to the vertical (Figure 1) by using a wooden square as a guide, and by burying the
containers up to the stem base and packing the earth firmly
around the pots. Leaning stems of the wind-treated block were
oriented in two directions along the axis of artificial wind: nine
saplings leaned into the wind and nine leaned away from the
wind (Figure 1). Leaning stems in the control block were oriented in cardinal directions (Figure 1). Trees were left in place
and stem growth movements analyzed during one growing
season, until removal for anatomical study on October 18,
1999.
Measurements of the stem profile
Stem growth response to a static (leaning) or a dynamic (wind)
load, or both, was recorded on May 15, i.e., 3 days after the beginning of the treatments, and on July 16 and October 17,
when the plants were harvested. Measurements were made
with a 3D Fastrak digitizer (Polhemus, acquisition software
Diplami by Sinoquet et al. 1997). With the transmitter as the
reference center, the digitizing sensor was slid upward along
one side of the stem and the Cartesian coordinates X, Y, Z registered every 10–15 mm, depending on the geometrical regularity of the stem. Data were obtained for the upper face of
leaning trees, the windward face of vertical wind-treated trees,
and the north-facing side of the vertical controls.
Calculation of the stem righting response
The successive three-dimensional (3D) profiles of a stem were
75
compared to quantify the reorientation process. First, the description and visualization of the successive stem profiles
were simplified by projecting the registered points on a vertical plane. The plane was defined by two points: the barycenter
of the three successive positions taken by the apex and the
equivalent for the stem base (Figure 2). Second, stem length
was calculated and the projected points were divided, depending on if they were in the lower, middle or upper third of the
stem. Then in a new 2D plot with horizontal and vertical axes,
linear regressions were made for each third of the stem and
slopes expressed as an angle to the vertical (θ) (Figure 2). Reorientation was quantified for any given third of a stem as the
decrease in that angle between two dates (∆θ) and the mean
value for the three thirds was considered the global stem righting response. Treatment effects were evaluated by analysis of
variance.
Basal dendrometry
Plants were harvested on October 18, 1999, final stem length
(L f) was measured, and discs taken from the stem base. Digital
photographs were taken of each disc. The geometry of the
discs beneath the bark—the vertical and horizontal diameters
(Df and df, respectively; Figure 3) and the surface areas of xylem and of any CW present (Af and Afcw, respectively; Figure 3)—were measured with image analysis software (IMAQ
Vision Builder, National Instruments, Austin, TX). Compression wood was easily identified by its characteristic brownto-red color (Timell 1986). Similar measurements were carried out on xylem that existed before the beginning of the experiment. The boundary of the existing xylem was clearly
marked by the previous year’s growth ring and by the lack of
CW. The vertical and horizontal diameters (Di and d i) and the
Figure 2. (a) Photograph of a Pinus
pinaster sapling taken in July showing
the righting response and (b)
quantitation of the reorientation of the
upper third of the stem throughout the
growing season, where a m and a o are
the slopes for the months of May and
October, respectively. Linear regressions were calculated for each stem
profile and slopes expressed as an angle to the vertical (θ).
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
76
BERTHIER AND STOKES
Primary growth index, R1, was calculated as:
R1 =
Lf − L i
Li
(6)
Secondary growth index, R2, was calculated as:
R2 =
Af − A i
Ai
(7)
The CW ratio, i.e., proportion of secondary growth dedicated to CW formation, was calculated as:
R CW =
Figure 3. Photograph of a stem cross section from an inclined tree
subjected to wind loading. Arrows indicate the directions in which
measurements were taken from the stem center to the boundary of the
annual growth ring in four directions. These growth rings have been
outlined. The stem was subjected to wind-loading from the lower side.
Compression wood (CW) formation and eccentric growth can be seen
on the upper side of the cross section (CW is outlined by a dotted
black line).
A f CW
Af − A i
(8)
Differences between treatments with respect to these stem
characteristics were compared by analysis of variance (Minitab).
Results
Plant performance and changes in stem lean
surface area of xylem (A i ) before treatment were also measured. The following stem characteristics were calculated:
Stem taper before treatment, Ti, was calculated as:
Ti =
Li
δi
(1)
Stem taper after treatment, Tf, was calculated as:
Tf =
Lf
δf
(2)
where A is either Ai used for Equation 1, or Af used for Equation 2:
 A

δ =2
 π 
(3)
Cross-sectional symmetry before treatment, Ci, was calculated as:
Ci =
Di
di
(4)
Cross-sectional symmetry after treatment, Cf, was calculated as:
Cf =
Df
df
(5)
After one growing season, no significant differences in R1 or
R2 were found between treatments (overall R1 = 2.61 ± 0.36;
overall R2 = 0.70 ± 0.06); however, a significant reduction in
stem taper was noted (Table 1). The basal stem section of the
vertical controls was essentially circular, whereas the basal
stem section of leaning plants became ovoid; however, the
change was not significant.
Stem profiles measured in July showed that trees that were
initially vertical remained vertical in both blocks, whereas
leaning trees had begun to straighten. The global righting response of the leaning trees did not differ significantly between
the blocks (Table 2). When the stems were divided into three
sections, it was found that the upper third of the stem followed
a similar rate of increase in reorientation in both blocks,
whereas the middle and basal thirds of the stem straightened
faster in the wind-treated block than in the control block (Table
2). No differences were found in the righting response between trees leaning toward and against the direction of wind
flow.
In October, trees that were initially vertical remained vertical, even when exposed to artificial wind, whereas leaning
trees showed significant global reorientation in both blocks,
Table 1. Changes in stem taper (T) and cross-sectional symmetry (C)
of basal stem sections in leaning Pinus pinaster saplings between
May (initial) and October (final). Data are means ± standard error.
T
C
TREE PHYSIOLOGY VOLUME 26, 2006
Initial
Final
P
8.5 ± 1.3
99.1 ± 9.1
7.2 ± 1.2
125.4 ± 16.8
0.005
< 0.001
RIGHTING RESPONSE OF WIND-LOADED, LEANING TREES
77
Table 2. Comparison of stem profiles of leaning control saplings and leaning, wind-treated saplings in July and October. Data are means ± standard
error. Abbreviation: ns = not significant at the 0.05 level.
Stem parts
Basal third
Median third
Apical third
Global response
July
P
Wind-treated
No wind
4.1 ± 3.2
8.1 ± 2.8
13.8 ± 4.6
8.7 ± 5.3
1.2 ± 3.2
5.2 ± 4.4
12.8 ± 4.6
6.4 ± 6.3
with individual values ranging from +12.5 to +29.0°. In addition, wind-treated trees showed a much faster overall straightening response than leaning controls, but this difference varied
among stem parts (Table 2): the upper third of the stem followed the same straightening pattern of +30.0 ± 3.0° in treated
and controlled trees, whereas the basal third showed a
4× greater response in the wind-treated saplings than the
controls. The middle third of the stem showed a slight difference between treatments, with a reorientation that was only
1.2× greater in wind-treated saplings than in controls. No significant differences in stem straightening occurred between
saplings leaning toward and against the direction of the artificial wind.
Compression wood formation
Compression wood was usually found in saplings from all
treatments, but was present in different amounts (Table 3).
When CW was expressed as a proportion of the growth-ring
surface, three distinct groups of trees were identified: the vertical controls with 3.8 ± 5.4% of CW, the vertical wind-treated
trees with 24.6 ± 7.0% of CW and all leaning trees, whether
wind-treated or not, with 49.1 ± 18.4% of CW (P < 0.001).
Discussion
The treatment differences in rate of stem straightening were
probably a consequence of the leaning angle and not growth
rate, because no differences in mean stem length or diameter
growth rate were observed between blocks. As predicted, leaning trees straightened irrespective of whether they were exposed to the wind treatment (Timell 1986, Kwon et al. 2001,
Plomion et al. 2001, Hellgren et al. 2004). However, although
our initial assumption was that trees growing along the direction of a prevailing wind would straighten less quickly than
0.05
0.05
ns
ns
October
P
Wind-treated
No wind
15.0 ± 5.3
23.0 ± 6.0
30.1 ± 3.0
22.7 ± 7.9
3.3 ± 5.1
18.8 ± 2.9
29.8 ± 3.2
17.3 ± 11.7
< 0.001
< 0.001
ns
< 0.005
those leaning into it, we found no difference in the righting response of trees leaning toward the wind compared with trees
leaning away from the wind. Trees subjected to unilateral mechanical perturbations, e.g., prevailing wind loading, can deflect permanently in the leeward direction (Telewski 1995).
Although the upper third of the stems of both leaning trees
and wind-treated leaning trees straightened at the same rate,
the righting response was significantly greater in the middle
and up to four times greater in the basal parts of stems of saplings subjected to wind loading, indicating that the dynamic
loads stimulated the righting response of the leaning saplings.
To our knowledge, this is the first time that such a response has
been observed in any plant species. The adaptive significance
of such a response is unknown.
The mechanism underlying the increase in the straightening
response in wind-loaded trees has yet to be determined. The
production of CW cannot explain the response because the
quantity of CW was not significantly different between control
and wind-treated plants. Given that CW formation is a gravitropic response, its efficiency in the stem righting process may
be influenced by other factors, e.g., mechanical perturbation.
Although we did not assess CW quality, certain characteristics
of CW that determine the amount of stem straightening, e.g.,
microfibril angle (Plomion et al. 2001) or lignin distribution
(Donaldson et al. 1999), may differ depending on the angle of
lean. If microfibril angle is also influenced by dynamic wind
loading, as shown by Telewski (1989), stem lean and dynamic
loading could result in a greater reaction in the newly developing cambial wood cells than stem lean alone.
Another hypothesis that might explain the increase in the
straightening response in leaning, wind-loaded trees is similar
to that proposed by Berthier and Stokes (2005) to account for
an increase in the phototropic response of maritime pine seedlings subjected to wind loading. In their experiment,
Table 3. Proportion of compression wood present in leaning (both with and without wind loading) Pinus pinaster saplings compared with vertical
saplings. Data are means ± standard error. Means followed by different letters differ significantly at P < 0.05; ns = not significant at the 0.05 level.
Wood
% Wood formation as a function of the previous year’s growth
Vertical trees
Secondary growth
Compression wood
P
Leaning trees
Control
Wind-treated
Control
Wind-treated
56.8 ± 16.1
3.8 ± 5.4 a
74.9 ± 37.6
24.6 ± 7.0 b
52.1 ± 19.2
46.9 ± 20.6 c
69.9 ± 34.7
50.6 ± 17.8 c
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
ns
< 0.005
78
BERTHIER AND STOKES
3-month-old wind-loaded seedlings showed increased heliotropism through greater stem lean toward the south, whereas
control seedlings remained straight. However, after 1 year, the
gravitropic effect dominated and stems straightened vertically,
with a significant decrease in the phototropic response. In both
our earlier study and the present one, dynamic wind loading
stimulated the tree response to the static load of stem lean and
this effect may improve tree dominance with respect to competition. The physiological response to wind stress is similar to
the gravitropic response, and it is likely that some of the same
genes are up-regulated by the two types of loading. Calcium
binding proteins and cell wall modifying enzymes are among
the functions to be potentially up-regulated by touch (Braam
2005). Consequently, concentrations of plant growth substances, ethylene and indole-3-acetic acid (IAA) may be altered
(Braam and Davis 1990, Du et al. 2004). Because windstressed plants were subjected to greater and more frequent
dynamic loads than the controls, it is possible that the stem
righting process was accelerated by increased enzyme and
hormone activity. However, Hellgren et al. (2004) showed that
IAA is not necessary for CW formation in stems and concluded that either signals other than IAA initiate reaction
wood formation, or that the gravitational stimulus interacts
with the IAA signal transduction pathway.
Berthier and Stokes (2005) suggested that cross-talk exists
between different sensory pathways in the cell, and that, by
stimulating mechanosensors through wind loading, several
other reactions may be induced in maritime pine seedlings, including phototropic bending. A common step that has been
identified in the transduction of a wide variety of signals
(Plieth and Trewavas 2002, Sanders et al. 2002), including
wind (Knight et al. 1992), is a rapid and transient elevation of
the free cytosolic calcium ion concentration ([Ca2+]cyt), which
has consequences for gene expression and downstream physiological processes, e.g., auxin regulation. The stimulated site
recovers initial sensitivity after only a short rest period (Correll and Kiss 2002, Plieth and Trewavas 2002), i.e., a recovery
time during which [Ca2+]cyt cannot be translocated as much or
as rapidly as previously. Acclimation or long-term sensitivity
adjustment can also occur in response to recurrent stimuli
(Trewavas 1999, Plieth and Trewavas 2002). Mechanosensitive Ca2+ channels have recently been found to exist in the
cell plasma membranes of Chara corallina and [Ca2+]cyt increases with an increase in mechanical stimulation (Kaneko et
al. 2005). A cytoskeletal structure, named the plasmalemmal
reticulum, is now thought to enhance signal transduction by
the cells’ mechanosensory Ca2+-selective cation channels in
BY-2 tobacco cells (Pickard and Fujiki 2005). There is also evidence suggesting that calcium is necessary for the formation
of gravity-stimulated CW (Du and Yamamoto 2003). If
[Ca2+]cyt is elevated frequently through dynamic loading and a
sufficiently long recovery time, i.e., the revolution period of
2 min in our experiment, plants may not only remain windsensitive, but CW formation will be enhanced in leaning
stems.
Acknowledgments
This work was supported by funding from SERFOB (Région Aquitaine), a Dufrenoy bursary and the Université Bordeaux I. Thanks are
due to P. Taris and J.L. Daban-Haurou who installed the wind device
as well as C. Plomion (INRA) for providing the plant material.
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