Directory UMM :Data Elmu:jurnal:T:Tree Physiology:vol17.1997:
Tree Physiology 17, 161--168
© 1997 Heron Publishing----Victoria, Canada
Evidence for red:far red signaling and photomorphogenic growth
response in Douglas-fir (Pseudotsuga menziesii) seedlings
GARY A. RITCHIE
The George R. Staebler Forest Resources Research Center, Weyerhaeuser Company, Centralia, WA 98531, USA
Received February 13, 1996
Summary In a greenhouse experiment, potted coastal
Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) seedlings
were grown in miniature ‘‘Nelder’’ (Nelder 1962) plots where
growing space varied from 265 to 2555 cm2 per plant. After
thirty weeks, mean plant height, crown biomass and branch
number increased significantly (P = 0.0141) with decreasing
growing space (increasing plant density). Differences in height
growth became apparent about six weeks after sowing. Furthermore, horizontally reflected radiation measured within the
Nelder plots showed a decrease in red:far-red ratio (R:FR) from
1.2 at the lowest density to 0.71 at the highest. Plant height was
strongly inversely correlated with estimated phytochrome photoequilibrium values (r 2 = 0.893). Field measurements made
in a three-year-old variable density plantation also showed a
decrease in R:FR with increasing planting density from 300 to
3,000 trees ha −1. These results support the hypothesis that
young Douglas-fir seedlings are able to detect, through the
phytochrome system, the presence of nearby seedlings owing
to the depletion of R relative to FR in the spectra reflected by
the foliage of the adjacent plants. They then adjust their growth
allometry in a way that reduces the possibility of being over
topped by these future competitors.
Keywords: competition, photomorphogenesis, phytochrome,
planting density, reforestation, shade avoidance.
Introduction
In young forest plantations, trees planted at high densities
frequently show more rapid height and diameter growth than
trees planted at low densities. The growth response (the ‘‘density effect’’) often manifests itself long before seedlings are tall
enough to shade one another, so it is not simply a response to
shade. It occurs even when competition from other species is
well controlled. The effect is ephemeral, typically lasting for a
few to several years, and has been observed in several species
(Cameron et al. 1991, DeBell and Giordano 1994, Knowe and
Hibbs 1996).
It has recently been reported that early height and diameter
growth of coastal Douglas-fir (Pseudotsuga menziesii (Mirb.)
Franco) seedlings also increase with planting density (Scott
et al. 1992, Scott et al., Weyerhaeuser Co., Federal Way WA,
unpublished results). They established 46 variable density test
plantations in western Washington and Oregon beginning in
1985. On each site, seedlings were planted at six densities,
ranging from about 3,000 trees ha −1 (2.0 m between seedlings)
to 300 trees ha −1 (5.8 m between seedlings). In winter 1990,
1,220 plots were established across the 11 oldest tests. Seedling height and stem diameter at breast height (DBH) were
measured in these plots. Taking the average seedling height at
the 3,000 trees ha −1 stocking density as 100%, heights of trees
at decreasing stocking densities were 91, 83, 85, 80 and 79%.
Comparable values for DBH were 100, 91, 83, 81, 76 and 67%.
Subsequent observations across the entire range of sites has
confirmed these early results. Height growth differences typically became visible during the third year after planting, when
the seedlings were less than 1 m tall, and well before they were
shaded by their neighbors.
The mechanism(s) triggering these differences in early
growth have not been elucidated. One recent hypothesis is that
plants are able to perceive the presence of nearby future competitors by sensing, through phytochrome, the spectral properties of the radiation reflected by the foliage of adjacent plants
(Ballaré et al. 1987, 1990, Smith et al. 1990, Ballaré et al. 1992,
1994, 1995). This radiation is depleted in the red (R; λ ~660
nm) region of the spectrum because of preferential absorption
of red light by chlorophyll. Far-red (FR; λ ~730 nm) radiation,
in contrast, is not diminished because virtually all FR incident
on foliage is reflected or transmitted (Smith 1994). Hence,
light reflected from foliage has a reduced R:FR ratio compared with solar radiation. The degree of reduction in incident
reflected R:FR is a function of the proximity or density, or
both, of competitors, thereby providing plants with an unequivocal ‘‘early warning signal’’ (Ballaré et al. 1987) of their
presence long before shading occurs.
It is well established that plants are able to perceive R:FR
radiation signals through the phytochrome system by means of
alterations in phytochrome photoequilibria (ϕ) (reviewed by
Mancinelli 1994) and to transduce these signals into photomorphogenic responses (Morgan et al. 1980, Schäfer and
Briggs 1986, Mohr 1988, Smith et al. 1990) through changes
in gene expression (Quail 1994, Quail et al. 1995). The first
demonstration of this effect in trees was in radiata pine (Pinus
radiata D. Don.) seedlings (Morgan et al. 1983). When exposed to artificial light with an altered R:FR ratio, these seedlings showed marked changes in the timing and intensity of
162
RITCHIE
flushing, shoot elongation and fasicle development. More recent work has suggested that phytochrome perception of R:FR
signals from neighboring trees may affect needle orientation in
Scots pine (Pinus sylvestris L.) (Galinski 1994). Gilbert and
coworkers (1995) provide convincing evidence that ϕ exerts a
strong influence on growth and crown architecture of poplar
(Populus trichocarpa × deltoides ‘Beaupré’).
This paper reports results of an experimental test of this
hypothesis with Douglas-fir seedlings that were grown in variable density plots in a greenhouse. Growth, biomass allocation
and R:FR responses to a density gradient were measured. In
addition, horizontally reflected R:FR radiation was monitored
in three-year-old Douglas-fir plantations planted at three densities.
Methods
Greenhouse experimental layout
The experiment was conducted in a commercial greenhouse in
Rochester, WA (lat. 46°75′ N, long. 123°20′ W, elev. 65m). The
layout was based on a Nelder (1962) fan design. Four fans,
each approximately 2.4 m square (Figure 1), were placed on
greenhouse benches that were covered with 0.6-cm mesh hardware cloth. Each fan contained 49 plastic pots (10 cm2 × 12 cm
deep). The fans had seven spokes, each 15° apart and radiating
from the origin. Pots were placed at successively greater distances (arcs) along the spokes so that plants in successive arcs
had progressively greater growing areas (Table 1). Spokes
were labeled ‘‘A’’ through ‘‘G’’, arcs were labeled ‘‘1’’ through
‘‘7’’. Pots in Spokes A and G and Arcs 1 and 7 contained border
plants that were not included in the measurements.
Plant culture
Douglas-fir seeds from a wild coastal Washington source were
stratified at 4 °C in early December 1994. Sterile pots were
filled with a mix comprising 1/1 (v/v) peat /perlite, and seeds
were sown, one per pot, on February 16, 1995. After sowing,
seeds were covered lightly with vermiculite to prevent drying
and were protected with bird netting. Under-bench heating
maintained the soil at about 18 °C during the germination
period. On March 28, 1995, immediately following seedling
emergence, the netting was removed and the fans were assembled. Seeds that did not emerge were replaced with seedlings
of the same seed lot that had been sown in reserve. Fans were
placed on the benches, and arrayed in random directions.
The plants were irrigated and fed every three days using a
commercial overhead boom irrigation system. This ensured
that all cultural treatments were applied evenly across the test.
Feeding was with a commercial fertilizer (N,P,K; 21,5,20) at
150 ppm N, alternated with calcium nitrate supplemental feed.
The greenhouse roof was a double layer of polyethylene film.
In early April, moss growth was observed colonizing the
surface of many of the pots. This was removed by hand and the
soil surface covered with grit to prevent further moss colonization.
Figure 1. Layout of one Nelder fan. Each square represents a pot
containing one seedling. There were seven arcs (‘‘1’’ through ‘‘7’’) and
seven spokes (‘‘A’’ through ‘‘G’’). Black dots indicate points at which
R:FR measurements were made. Plant areas were estimated as shown
in the cross-hatched area. Plants in Spokes ‘‘A’’ and ‘‘G’’ and in Arcs
‘‘1’’ and ‘‘7’’ were considered border plants and were not included in
data analysis.
Table 1. Distance of each plant from the origin, distance from the
previous plant, and growing area per plant in each Nelder fan.
Arc
Distance
from
origin (m)
Distance from
previous
arc (m)
Area per
plant
cm2
1
2
3
4
5
6
7
0.457
0.610
0.808
1.067
1.387
1.829
2.438
-0.152
0.198
0.259
0.320
0.472
0.610
-265
490
826
1432
2555
--
Measurements and harvest
Plant height was measured on all seedlings in Spokes B and F
of all four fans every other week after sowing. Only two spokes
were measured to avoid confounding the experiment by excessive touching of the plants (Braam and Davis 1990). Two
measurements were made. The first was from the soil line to
the base of the cotyledons (hypocotyls). The second measure
was taken from the cotyledons to the growing tip (epicotyls).
Plants in three fans were harvested during the week of
September 15, 1995. At that time, total plant height, stem
diameter (two measurements averaged), number of branches,
oven dry weight of plant top, oven dry weight of root system,
and total oven dry weight of branches were determined. Total
plant weight and root:shoot ratio were calculated from these
RED:FAR RED SIGNALING AND GROWTH RESPONSE IN DOUGLAS-FIR
measurements. Several of the plants exhibited abnormal,
stunted, development. These were noted on the data sheets and
their measurements were not included in the analysis. One fan
was retained for subsequent spectral measurements.
Spectral measurements
From August through October 1995 a recently calibrated LI1800 spectroradiometer (Li-Cor, Inc., Lincoln, NE) fitted with
an integrating cylinder (Ballaré et al. 1987) with a ± 10°
acceptance angle was used to measure horizontally reflected
radiation spectra coming from 360° at the intersect of each arc
along Spoke D of Fan 3 (black dots in Figure 1). The integrating cylinder was used because measurements made with traditional cosine corrected planar sensors do not adequately
characterize the radiation conditions at the photoreceptive sites
in even-aged plant populations (Ballaré et al. 1990). The procedure was to remove each plant from its position and to
replace it with the sensor, which was located at roughly midcrown height ~ 15--20 cm above the bench surface. Then a
triple scan was run at 5-nm band intervals from 400 to 800 nm.
The R:FR ratio was calculated as the ratio of photon irradiance
in the bands at 655--665 nm (R) over irradiance in the bands
725--735 nm (FR) (Smith 1994). A black shroud was placed
between the sensor and the persons making the measurements
to prevent their presence from being sensed. During the August
measurements, the sensor tip was accidentally chipped. A new
tip was fabricated and used to make additional measurements
at the same positions during October.
Data analysis
Initially, scatter plots were constructed with the raw data, in
which each dependent variable was plotted against the plant
growing area, which served as a surrogate for plant growing
density (greater area = lower density). These plots revealed that
the relationships tended to be logarithmic. Therefore, the plant
growing areas were log transformed and subjected to linear
regression analysis using the model: dependent variable = a +
b log(plant area).
These analyses yielded P and r 2 values for each regression.
Regressions were evaluated by plotting residuals against expected values. These analyses were conducted with pooled
data from all three fans.
163
trees ha −1), medium density (1,400 trees ha −1) and high density
(3,000 trees ha −1) blocks. In each case, the tripod-mounted
sensor was placed directly over the top of one seedling.
Shorter-than-average seedlings were selected so that the sensor
could be placed at roughly mid-crown for trees of average
height, which was about 0.75 m. The instrument was programed to perform triple scans, which were averaged. Scans were
run on several occasions in the high, medium, and low density
blocks to gain information on spectral properties associated
with stand density. The R:FR ratios were calculated as described above.
Results
Greenhouse experiment
Twenty-one trees were stunted (about 11% of total). Fifteen
were in Fan 1, with Fan 2 and Fan 4 having only three each.
There was no pattern to the distribution of stunted trees within
fans. The reason for stunting is unknown, but it could have
reflected seed size or vigor, or mutation. Stunted tree measurements were removed from the data base before analysis.
The slopes of the linear regressions on log(area) were significant for height, number of branches, top weight, and
root:shoot ratio (Table 2). Among these, residual analyses were
acceptable for all except branch number, where there was an
indication of unequal variance. The decrease in plant height
with increasing growing area (decreasing plant density) is
shown in Figure 2 (all points shown). Virtually all of the height
growth difference occurred in the epicotyls. A log curve of the
type y = a + bln (x) was fitted through the regression. Mean
height, mean branch number and mean top dry weight decreased with increasing growing area in a similar manner
(Figure 3). In contrast, the relationship of root:shoot ratio to
growing area gave a positive slope, indicating that top growth
increased relative to root growth as density increased (Figure 4).
The ratio of R:FR radiation decreased as plant density increased (Figure 5). Some differences in the absolute values of
R:FR across measurement dates were observed. These may
have reflected differences in plant size, sun angle, sky conditions, or the change in sensor tips. Nevertheless, the trend was
Field measurements
A variable density plantation had been established during
February and March 1993 on an Astoria soil at Marcuson
Creek near Dryad, WA (lat. 46°54′ N, long. 123°25′ W, elev.
125 m). One set of 0.4-ha blocks contained two-year-old
Douglas-fir (transplanted (1 + 1) nursery stock) planted at 300,
1,400 and 3,000 trees ha −1. Before planting, the site had been
sprayed to eliminate brush competition and fenced to prevent
browsing by big game and rabbits. Brush was controlled by
hand cutting during the three growing seasons following planting. The site index (50-year height) was about 43 m.
The Li-Cor spectroradiometer with integrating cylinder was
used to measure horizontally reflected R:FR radiation on several days during the growing season in the low density (300
Table 2. Linear regressions of dependent variables on plant growing
area (log transformed).
Dependent
variable
Intercept Slope
Height
555.5
Diameter
5.35
No. branches
32.9
Top dry wt.
3.56
Root dry wt.
4.15
Total dry wt.
7.709
Branch dry wt. 5.52
Root/Shoot
0.707
1
− 33.9
0.01
− 1.43
− 0.204
0.176
− 0.028
0.01
0.265
a = Evidence of unequal variance.
P
r2
Residuals
0.0009
0.9046
0.0458
0.0175
0.5167
0.9287
0.9581
0.0207
0.1639
0.0002
0.0628
0.0877
0.0068
0.0001
0.0000
0.0834
OK
OK
a1
OK
a
OK
OK
OK
164
RITCHIE
Figure 2. Final heights of individual Douglas-fir seedlings in all fans
combined, as a function of plant growing area. Measurements were
made approximately 205 days after seeds were sown. Log curve was
fitted and plotted by computer.
Figure 5. The R:FR ratios of horizontally reflected radiation measured
at five positions in a Nelder ‘‘fan’’ (see Figure 1). The August 23,
October 26 overcast and October 26 sunny measurements were made
at 1000, 1030 and 1130 h, respectively. Each point is a mean of three
scans.
always for a logarithmic increase in R:FR with decrease in
plant density.
Trends in R:FR in the field
Figure 3. Means (± 1 SE) of Douglas-fir seedling height, branch
number, and top dry weight as a function of growing area. Data were
collected approximately 205 days after seeds were sown. Log curve
was fitted and plotted by computer.
Figure 4. Mean root/shoot ratios of Douglas-fir seedlings growing in
all fans combined as a function of plant growing area. Measurements
were made approximately 205 days after sowing. Log curve was fitted
and plotted by computer.
Three patterns emerged from field measurements of horizontal
R:FR radiation. First, R:FR varied diurnally, being high at
dawn and dusk and reaching a daily minimum value during
midday. Second, sky conditions affected R:FR. Diurnal curves
were smooth on clear days and less so on cloudy or rainy days.
The midday minima were often lower on clear, sunny days
than on cloudy, rainy days. Finally, regardless of sky conditions, R was depleted relative to FR with increasing density
(e.g., at midday on May 24, 1995, R:FR = 1.038, 0.939 and
0.792 at 300, 1,400 and 3,000 trees ha −1, respectively).
Discussion
This work was undertaken to gain a clearer understanding of
the mechanism(s) that trigger the density effect in young
Douglas-fir plantations. Several hypotheses have been suggested to explain the higher early growth rates associated with
higher planting densities including the following.
(1) Animal browsing Assuming a relatively constant number of
browsing animals in a given setting, a high-density plantation
would have a lower ratio of animals to seedlings than a lowdensity plantation and would, presumably, suffer less browsing.
(2) Weed and brush competition Stands of trees planted at high
densities would capture the site and its resources more rapidly
compared with low-density stands. This would impede the
development of weed communities and result in faster early
tree growth.
(3) Mycorrhizal associations Most forest trees, including
Douglas-fir, form mycorrhizal associations. A dense plantation
might form more rapid connections among tree roots and
mycorrhizal hyphae than a sparse plantation (Perry et al. 1992,
RED:FAR RED SIGNALING AND GROWTH RESPONSE IN DOUGLAS-FIR
Amaranthus and Perry 1994), hence providing more carbon for
the mycorrhizal mat and promoting its growth and vigor. This
would result in greater benefits to the trees and more rapid
early growth.
(4) Root grafting Root grafting would occur sooner in dense
plantings than in sparse plantings. Trees could then share and
exploit site resources more efficiently and early growth would
be enhanced.
(5) Nitrogen mineralization Compared to roots in a sparse
plantation, roots in a dense plantation would exploit the rhizosphere more rapidly and increase the rate of nitrogen mineralization, through root exudates, leading to more rapid early
tree growth.
(6) Perception and avoidance of future competition Trees
growing in close proximity with other trees are able to ‘‘perceive’’ the presence of these future competitors. This is followed by a change in growth programing that focuses on
height growth in order to avoid overshadowing (Aphalo and
Ballaré 1995). The mechanism of perception might be through
R:FR signaling, or by root contact (Mahall and Callaway
1991).
This experiment failed to reject hypothesis No. 6 as it related
to R:FR signaling. However, it did not test whether root interactions, competing brush, or animals have effects on early
height growth in young stands. Further research will be required to determine the significance of these potential effects.
Despite the fact that the Nelder variable density planting was
carried out in miniature in a greenhouse, its results are in
concert with both the field observations of Scott et al. (1992)
and with ‘‘growth waves’’ often observed in full-scale field
Nelder plantings (Figure 6). In the field, increases occurred in
height and stem diameter. In the greenhouse, height, branch
number, and top weight increased, whereas stem diameter did
not. However, if diameters varied across densities in the same
165
proportion as heights (about 10%), then the maximum differences in diameter would have been on the order of only
0.5 mm. It is possible that the hand method used to measure
stem diameter may not have been of sufficient precision to
detect differences at this scale.
Results of both greenhouse and field measurements of R:FR
radiation supported the R:FR signaling hypothesis. In both
cases, R was depleted relative to FR as plant density increased.
Differences in R:FR are perceived by the plant through the
phytochrome system. Evidence from a wide range of plants
species (summarized by Smith 1982, 1994) indicates that stem
extension (height) growth is linearly and negatively related to
phytochrome photoequilibrium (ϕ):
ϕ = Pfr /P,
(1)
where Pfr is the phytochrome fraction in the far-red absorbing
form, and P is the total phytochrome.
To test this with the height data obtained from the greenhouse study, ϕ values were estimated from the R:FR values
measured on August 23 (Figure 5, August 23 values) based on
the relationship provided by Smith (1982, Figure 2). Plant
height, plotted as a function of estimated ϕ, yielded the predicted linear relationship with a strong negative slope (Figure 7) providing further support for the interpretation that the
observed growth response was mediated by phytochrome.
Once the R:FR signal is perceived and transduced, plants
presumably alter their internal growth program in such a manner as to gain greater light harvesting ability in crowded situations (i.e., greater height) and improve their competitive
position. This might occur by increasing the efficiency of
either carbon assimilation or use, or both, or by changing
carbon allocation patterns, or both. The final plant biomass
distributions across the six densities provide insight as to what
Figure 6. An aerial photograph
of two side-by-side, five-yearold Nelder test plots near
Turner, Oregon. At this time,
trees growing near the center
of the plots, at high densities,
were showing considerably
greater height (and diameter)
growth than trees growing in
the outside rows. Over time
these ‘‘growth waves’’ typically move outward. Photograph was taken in 1978,
photographer is unknown.
166
RITCHIE
Figure 7. Relationship of Douglas-fir seedling final height to estimated
phytochrome photoequilibria. Numbers in parentheses are arc numbers from the origin of the Nelder fan. Each point is a mean ± 1 SE of
all plants from all fans (about 25 plants per point).
may have occurred in the greenhouse study. Root weights
decreased and total plant weights remained relatively constant,
whereas top weights increased with density, resulting in a
decreasing root:shoot ratio (Figure 4). This suggests that an
increase in carbon allocation to above-ground parts, relative to
below ground parts, may have occurred as a response to the
R:FR signals and altered ϕ. This is consistent with observations on soybean (Glycene max (L.) Merr.) (Kasperbauer
1987), and red beet (Beta vulgaris L.) (Hole et al. 1984).
Other interpretations of these results cannot be ruled out,
however. It is possible, for example, that subtle gradients in
temperature, vapor pressure deficit, air movement, or other
factors could have occurred within the fans and might have
been implicated in the observed growth responses. However,
this does not seem likely for the following reason. Weekly
height measurements begun when the seedlings were just
emerging from the cotyledon stage are shown in Figure 8.
These growth curves show that the seedlings in Arcs 2 (highest
density) and 6 (lowest density) were beginning to differentiate
themselves from those in the other arcs as early as 45 days after
sowing when the seedlings were only about 5.5 cm tall. It
seems unlikely that, at this diminutive size, they could have
modified the environment around seedlings growing 15 cm
away sufficiently to cause them to alter their growth patterns.
Nevertheless, this explanation cannot be discounted without
further experimentation.
If the density effect evident in the field trials is, in fact,
triggered by R:FR signaling among seedlings, it represents a
considerable extension of the reported physical distances
across which such signals are perceived. Field measurements
of R:FR were made at various distances from artificial canopies constructed of tobacco (Nicotiana tobacum L.) or mustard
(Sinapis alba L.) plants with a spectroradiometer equipped
with a cosine corrected sensor (Smith et al. 1990). Red depletion and far-red enhancement were detected at a maximum
Figure 8. Height growth curves for Douglas-fir seedlings from Spokes
‘‘B’’ and ‘‘F’’ in across four fans beginning when seedlings had just
emerged from the cotyledon stage. Plants in Arc 2 are growing at the
highest density, whereas those in Arc 6 are at the lowest density.
distance of 30 cm from these canopies. If R:FR signaling is
triggering the density effect in our plantations, these signals
must be propagated for a distance of at least 6 m, for that is the
distance between seedlings planted at 3,000 trees ha −1. Independent measurements, made with the integrating cylinder
adjacent to a 2.5-m-tall Douglas-fir hedge, showed a measurable R depletion and FR enhancement out to approximately
3 m from the hedge (unpublished data).
A perplexing question that bears on this interpretation involves the role of lesser vegetation. Presumably such plants
would also deplete red light energy, depressing the R:FR
reflected from their foliage and sending ‘‘false signals’’ to the
Douglas-fir seedlings. How would Douglas-fir seedlings discriminate among signals from plants that do not represent
potential competitors and those that do (i.e., other tree species)? Several possible explanations come to mind. First, signal timing may be important. Trees may be sensitive to the
R:FR signal only during early spring, when their shoots are
elongating, but before weeds and deciduous plants are in full
leaf. Five-minute exposure of soybean plants to altered R:FR
was sufficient to induce changes in morphogenesis (Kasperbauer 1987), and elongating shoots are apparently the sites of
R:FR perception in other species (Morgan et al. 1980, Child
and Smith 1987, Ballaré et al. 1990). Alternatively, the phytochrome mechanism may be sufficiently sophisticated to discriminate among the reflectance properties of the leaves
(Woolley 1971, Lee and Graham 1986) of different plants.
Phytochrome is not a single molecular species, but is comprised of a broad family of photoreceptors encoded by multiple
divergent genes (Quail 1994). To complicate matters further,
the ability of some plants to respond to phytochrome is dependent on the presence of blue or ultraviolet (UV-A) light
(Mohr 1994). Such ‘‘coaction’’ between plant pigment systems
has been demonstrated in Scots pine seedlings by Fernbach
and Mohr (1990). Such richness of information-gathering
RED:FAR RED SIGNALING AND GROWTH RESPONSE IN DOUGLAS-FIR
leads to speculation that not only detection, but identification,
of neighboring plants might be occurring in nature.
From a practical standpoint, the growth promoting effects of
R:FR signaling can be exploited in forest management by
increasing planting density and developing early thinning and
silvicultural prescriptions to maintain proper stocking densities. This is now being done in certain areas of the coastal
Pacific Northwest. It is doubtful that greenhouse or nursery
production could be enhanced, however, because typical growing densities are already capturing the density effect.
The implications of this phenomenon to modeling competition in forest stands are obvious. The incorporation into such
models, of algorithms simulating sophisticated informationgathering systems (Aphalo and Ballaré 1995) such as R:FR
signaling, would tend to enhance their predictive ability beyond that of models based solely on passive plant responses to
resource limitations. This could lead to fundamentally new
ways of thinking about the biology of plant competition and
interaction, and should stimulate a great deal of additional
research.
Acknowledgments
The capable technical assistance of James Keeley and Patty Ward is
gratefully acknowledged. I also appreciate the generous cooperation
of the Weyerhaeuser Company Rochester Regeneration Center staff in
growing plants and for providing space to conduct this study. I thank
Dr. Carlos Ballaré, University of Buenos Aires, Argentina for advice
and for providing a prototype of the integrating cylinder used in the
spectroradiometric measurements. Weyerhaeuser colleagues Drs.
Wm. Scott, Roger Timmis, Christine Dean, Wm. Carlson, and Peter
Farnum, along with Steven Duke and Paul Figueroa reviewed earlier
drafts of this paper. Drs. R. van den Driessche, R. Guy, C. Harrington,
T. Terry and R. Edmonds contributed to hypothesis development. Prof.
Harry Smith, Univ. of Leicester, UK, and two anonymous referees
provided reviews of the submission manuscript. A special thank you
to Dr. Barbara Yoder, Oregon State University, who planted the early
ideas for this work and provided me with two seminal papers on the
topic of R:FR signaling. This research and its publication were supported by Weyerhaeuser Company.
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© 1997 Heron Publishing----Victoria, Canada
Evidence for red:far red signaling and photomorphogenic growth
response in Douglas-fir (Pseudotsuga menziesii) seedlings
GARY A. RITCHIE
The George R. Staebler Forest Resources Research Center, Weyerhaeuser Company, Centralia, WA 98531, USA
Received February 13, 1996
Summary In a greenhouse experiment, potted coastal
Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) seedlings
were grown in miniature ‘‘Nelder’’ (Nelder 1962) plots where
growing space varied from 265 to 2555 cm2 per plant. After
thirty weeks, mean plant height, crown biomass and branch
number increased significantly (P = 0.0141) with decreasing
growing space (increasing plant density). Differences in height
growth became apparent about six weeks after sowing. Furthermore, horizontally reflected radiation measured within the
Nelder plots showed a decrease in red:far-red ratio (R:FR) from
1.2 at the lowest density to 0.71 at the highest. Plant height was
strongly inversely correlated with estimated phytochrome photoequilibrium values (r 2 = 0.893). Field measurements made
in a three-year-old variable density plantation also showed a
decrease in R:FR with increasing planting density from 300 to
3,000 trees ha −1. These results support the hypothesis that
young Douglas-fir seedlings are able to detect, through the
phytochrome system, the presence of nearby seedlings owing
to the depletion of R relative to FR in the spectra reflected by
the foliage of the adjacent plants. They then adjust their growth
allometry in a way that reduces the possibility of being over
topped by these future competitors.
Keywords: competition, photomorphogenesis, phytochrome,
planting density, reforestation, shade avoidance.
Introduction
In young forest plantations, trees planted at high densities
frequently show more rapid height and diameter growth than
trees planted at low densities. The growth response (the ‘‘density effect’’) often manifests itself long before seedlings are tall
enough to shade one another, so it is not simply a response to
shade. It occurs even when competition from other species is
well controlled. The effect is ephemeral, typically lasting for a
few to several years, and has been observed in several species
(Cameron et al. 1991, DeBell and Giordano 1994, Knowe and
Hibbs 1996).
It has recently been reported that early height and diameter
growth of coastal Douglas-fir (Pseudotsuga menziesii (Mirb.)
Franco) seedlings also increase with planting density (Scott
et al. 1992, Scott et al., Weyerhaeuser Co., Federal Way WA,
unpublished results). They established 46 variable density test
plantations in western Washington and Oregon beginning in
1985. On each site, seedlings were planted at six densities,
ranging from about 3,000 trees ha −1 (2.0 m between seedlings)
to 300 trees ha −1 (5.8 m between seedlings). In winter 1990,
1,220 plots were established across the 11 oldest tests. Seedling height and stem diameter at breast height (DBH) were
measured in these plots. Taking the average seedling height at
the 3,000 trees ha −1 stocking density as 100%, heights of trees
at decreasing stocking densities were 91, 83, 85, 80 and 79%.
Comparable values for DBH were 100, 91, 83, 81, 76 and 67%.
Subsequent observations across the entire range of sites has
confirmed these early results. Height growth differences typically became visible during the third year after planting, when
the seedlings were less than 1 m tall, and well before they were
shaded by their neighbors.
The mechanism(s) triggering these differences in early
growth have not been elucidated. One recent hypothesis is that
plants are able to perceive the presence of nearby future competitors by sensing, through phytochrome, the spectral properties of the radiation reflected by the foliage of adjacent plants
(Ballaré et al. 1987, 1990, Smith et al. 1990, Ballaré et al. 1992,
1994, 1995). This radiation is depleted in the red (R; λ ~660
nm) region of the spectrum because of preferential absorption
of red light by chlorophyll. Far-red (FR; λ ~730 nm) radiation,
in contrast, is not diminished because virtually all FR incident
on foliage is reflected or transmitted (Smith 1994). Hence,
light reflected from foliage has a reduced R:FR ratio compared with solar radiation. The degree of reduction in incident
reflected R:FR is a function of the proximity or density, or
both, of competitors, thereby providing plants with an unequivocal ‘‘early warning signal’’ (Ballaré et al. 1987) of their
presence long before shading occurs.
It is well established that plants are able to perceive R:FR
radiation signals through the phytochrome system by means of
alterations in phytochrome photoequilibria (ϕ) (reviewed by
Mancinelli 1994) and to transduce these signals into photomorphogenic responses (Morgan et al. 1980, Schäfer and
Briggs 1986, Mohr 1988, Smith et al. 1990) through changes
in gene expression (Quail 1994, Quail et al. 1995). The first
demonstration of this effect in trees was in radiata pine (Pinus
radiata D. Don.) seedlings (Morgan et al. 1983). When exposed to artificial light with an altered R:FR ratio, these seedlings showed marked changes in the timing and intensity of
162
RITCHIE
flushing, shoot elongation and fasicle development. More recent work has suggested that phytochrome perception of R:FR
signals from neighboring trees may affect needle orientation in
Scots pine (Pinus sylvestris L.) (Galinski 1994). Gilbert and
coworkers (1995) provide convincing evidence that ϕ exerts a
strong influence on growth and crown architecture of poplar
(Populus trichocarpa × deltoides ‘Beaupré’).
This paper reports results of an experimental test of this
hypothesis with Douglas-fir seedlings that were grown in variable density plots in a greenhouse. Growth, biomass allocation
and R:FR responses to a density gradient were measured. In
addition, horizontally reflected R:FR radiation was monitored
in three-year-old Douglas-fir plantations planted at three densities.
Methods
Greenhouse experimental layout
The experiment was conducted in a commercial greenhouse in
Rochester, WA (lat. 46°75′ N, long. 123°20′ W, elev. 65m). The
layout was based on a Nelder (1962) fan design. Four fans,
each approximately 2.4 m square (Figure 1), were placed on
greenhouse benches that were covered with 0.6-cm mesh hardware cloth. Each fan contained 49 plastic pots (10 cm2 × 12 cm
deep). The fans had seven spokes, each 15° apart and radiating
from the origin. Pots were placed at successively greater distances (arcs) along the spokes so that plants in successive arcs
had progressively greater growing areas (Table 1). Spokes
were labeled ‘‘A’’ through ‘‘G’’, arcs were labeled ‘‘1’’ through
‘‘7’’. Pots in Spokes A and G and Arcs 1 and 7 contained border
plants that were not included in the measurements.
Plant culture
Douglas-fir seeds from a wild coastal Washington source were
stratified at 4 °C in early December 1994. Sterile pots were
filled with a mix comprising 1/1 (v/v) peat /perlite, and seeds
were sown, one per pot, on February 16, 1995. After sowing,
seeds were covered lightly with vermiculite to prevent drying
and were protected with bird netting. Under-bench heating
maintained the soil at about 18 °C during the germination
period. On March 28, 1995, immediately following seedling
emergence, the netting was removed and the fans were assembled. Seeds that did not emerge were replaced with seedlings
of the same seed lot that had been sown in reserve. Fans were
placed on the benches, and arrayed in random directions.
The plants were irrigated and fed every three days using a
commercial overhead boom irrigation system. This ensured
that all cultural treatments were applied evenly across the test.
Feeding was with a commercial fertilizer (N,P,K; 21,5,20) at
150 ppm N, alternated with calcium nitrate supplemental feed.
The greenhouse roof was a double layer of polyethylene film.
In early April, moss growth was observed colonizing the
surface of many of the pots. This was removed by hand and the
soil surface covered with grit to prevent further moss colonization.
Figure 1. Layout of one Nelder fan. Each square represents a pot
containing one seedling. There were seven arcs (‘‘1’’ through ‘‘7’’) and
seven spokes (‘‘A’’ through ‘‘G’’). Black dots indicate points at which
R:FR measurements were made. Plant areas were estimated as shown
in the cross-hatched area. Plants in Spokes ‘‘A’’ and ‘‘G’’ and in Arcs
‘‘1’’ and ‘‘7’’ were considered border plants and were not included in
data analysis.
Table 1. Distance of each plant from the origin, distance from the
previous plant, and growing area per plant in each Nelder fan.
Arc
Distance
from
origin (m)
Distance from
previous
arc (m)
Area per
plant
cm2
1
2
3
4
5
6
7
0.457
0.610
0.808
1.067
1.387
1.829
2.438
-0.152
0.198
0.259
0.320
0.472
0.610
-265
490
826
1432
2555
--
Measurements and harvest
Plant height was measured on all seedlings in Spokes B and F
of all four fans every other week after sowing. Only two spokes
were measured to avoid confounding the experiment by excessive touching of the plants (Braam and Davis 1990). Two
measurements were made. The first was from the soil line to
the base of the cotyledons (hypocotyls). The second measure
was taken from the cotyledons to the growing tip (epicotyls).
Plants in three fans were harvested during the week of
September 15, 1995. At that time, total plant height, stem
diameter (two measurements averaged), number of branches,
oven dry weight of plant top, oven dry weight of root system,
and total oven dry weight of branches were determined. Total
plant weight and root:shoot ratio were calculated from these
RED:FAR RED SIGNALING AND GROWTH RESPONSE IN DOUGLAS-FIR
measurements. Several of the plants exhibited abnormal,
stunted, development. These were noted on the data sheets and
their measurements were not included in the analysis. One fan
was retained for subsequent spectral measurements.
Spectral measurements
From August through October 1995 a recently calibrated LI1800 spectroradiometer (Li-Cor, Inc., Lincoln, NE) fitted with
an integrating cylinder (Ballaré et al. 1987) with a ± 10°
acceptance angle was used to measure horizontally reflected
radiation spectra coming from 360° at the intersect of each arc
along Spoke D of Fan 3 (black dots in Figure 1). The integrating cylinder was used because measurements made with traditional cosine corrected planar sensors do not adequately
characterize the radiation conditions at the photoreceptive sites
in even-aged plant populations (Ballaré et al. 1990). The procedure was to remove each plant from its position and to
replace it with the sensor, which was located at roughly midcrown height ~ 15--20 cm above the bench surface. Then a
triple scan was run at 5-nm band intervals from 400 to 800 nm.
The R:FR ratio was calculated as the ratio of photon irradiance
in the bands at 655--665 nm (R) over irradiance in the bands
725--735 nm (FR) (Smith 1994). A black shroud was placed
between the sensor and the persons making the measurements
to prevent their presence from being sensed. During the August
measurements, the sensor tip was accidentally chipped. A new
tip was fabricated and used to make additional measurements
at the same positions during October.
Data analysis
Initially, scatter plots were constructed with the raw data, in
which each dependent variable was plotted against the plant
growing area, which served as a surrogate for plant growing
density (greater area = lower density). These plots revealed that
the relationships tended to be logarithmic. Therefore, the plant
growing areas were log transformed and subjected to linear
regression analysis using the model: dependent variable = a +
b log(plant area).
These analyses yielded P and r 2 values for each regression.
Regressions were evaluated by plotting residuals against expected values. These analyses were conducted with pooled
data from all three fans.
163
trees ha −1), medium density (1,400 trees ha −1) and high density
(3,000 trees ha −1) blocks. In each case, the tripod-mounted
sensor was placed directly over the top of one seedling.
Shorter-than-average seedlings were selected so that the sensor
could be placed at roughly mid-crown for trees of average
height, which was about 0.75 m. The instrument was programed to perform triple scans, which were averaged. Scans were
run on several occasions in the high, medium, and low density
blocks to gain information on spectral properties associated
with stand density. The R:FR ratios were calculated as described above.
Results
Greenhouse experiment
Twenty-one trees were stunted (about 11% of total). Fifteen
were in Fan 1, with Fan 2 and Fan 4 having only three each.
There was no pattern to the distribution of stunted trees within
fans. The reason for stunting is unknown, but it could have
reflected seed size or vigor, or mutation. Stunted tree measurements were removed from the data base before analysis.
The slopes of the linear regressions on log(area) were significant for height, number of branches, top weight, and
root:shoot ratio (Table 2). Among these, residual analyses were
acceptable for all except branch number, where there was an
indication of unequal variance. The decrease in plant height
with increasing growing area (decreasing plant density) is
shown in Figure 2 (all points shown). Virtually all of the height
growth difference occurred in the epicotyls. A log curve of the
type y = a + bln (x) was fitted through the regression. Mean
height, mean branch number and mean top dry weight decreased with increasing growing area in a similar manner
(Figure 3). In contrast, the relationship of root:shoot ratio to
growing area gave a positive slope, indicating that top growth
increased relative to root growth as density increased (Figure 4).
The ratio of R:FR radiation decreased as plant density increased (Figure 5). Some differences in the absolute values of
R:FR across measurement dates were observed. These may
have reflected differences in plant size, sun angle, sky conditions, or the change in sensor tips. Nevertheless, the trend was
Field measurements
A variable density plantation had been established during
February and March 1993 on an Astoria soil at Marcuson
Creek near Dryad, WA (lat. 46°54′ N, long. 123°25′ W, elev.
125 m). One set of 0.4-ha blocks contained two-year-old
Douglas-fir (transplanted (1 + 1) nursery stock) planted at 300,
1,400 and 3,000 trees ha −1. Before planting, the site had been
sprayed to eliminate brush competition and fenced to prevent
browsing by big game and rabbits. Brush was controlled by
hand cutting during the three growing seasons following planting. The site index (50-year height) was about 43 m.
The Li-Cor spectroradiometer with integrating cylinder was
used to measure horizontally reflected R:FR radiation on several days during the growing season in the low density (300
Table 2. Linear regressions of dependent variables on plant growing
area (log transformed).
Dependent
variable
Intercept Slope
Height
555.5
Diameter
5.35
No. branches
32.9
Top dry wt.
3.56
Root dry wt.
4.15
Total dry wt.
7.709
Branch dry wt. 5.52
Root/Shoot
0.707
1
− 33.9
0.01
− 1.43
− 0.204
0.176
− 0.028
0.01
0.265
a = Evidence of unequal variance.
P
r2
Residuals
0.0009
0.9046
0.0458
0.0175
0.5167
0.9287
0.9581
0.0207
0.1639
0.0002
0.0628
0.0877
0.0068
0.0001
0.0000
0.0834
OK
OK
a1
OK
a
OK
OK
OK
164
RITCHIE
Figure 2. Final heights of individual Douglas-fir seedlings in all fans
combined, as a function of plant growing area. Measurements were
made approximately 205 days after seeds were sown. Log curve was
fitted and plotted by computer.
Figure 5. The R:FR ratios of horizontally reflected radiation measured
at five positions in a Nelder ‘‘fan’’ (see Figure 1). The August 23,
October 26 overcast and October 26 sunny measurements were made
at 1000, 1030 and 1130 h, respectively. Each point is a mean of three
scans.
always for a logarithmic increase in R:FR with decrease in
plant density.
Trends in R:FR in the field
Figure 3. Means (± 1 SE) of Douglas-fir seedling height, branch
number, and top dry weight as a function of growing area. Data were
collected approximately 205 days after seeds were sown. Log curve
was fitted and plotted by computer.
Figure 4. Mean root/shoot ratios of Douglas-fir seedlings growing in
all fans combined as a function of plant growing area. Measurements
were made approximately 205 days after sowing. Log curve was fitted
and plotted by computer.
Three patterns emerged from field measurements of horizontal
R:FR radiation. First, R:FR varied diurnally, being high at
dawn and dusk and reaching a daily minimum value during
midday. Second, sky conditions affected R:FR. Diurnal curves
were smooth on clear days and less so on cloudy or rainy days.
The midday minima were often lower on clear, sunny days
than on cloudy, rainy days. Finally, regardless of sky conditions, R was depleted relative to FR with increasing density
(e.g., at midday on May 24, 1995, R:FR = 1.038, 0.939 and
0.792 at 300, 1,400 and 3,000 trees ha −1, respectively).
Discussion
This work was undertaken to gain a clearer understanding of
the mechanism(s) that trigger the density effect in young
Douglas-fir plantations. Several hypotheses have been suggested to explain the higher early growth rates associated with
higher planting densities including the following.
(1) Animal browsing Assuming a relatively constant number of
browsing animals in a given setting, a high-density plantation
would have a lower ratio of animals to seedlings than a lowdensity plantation and would, presumably, suffer less browsing.
(2) Weed and brush competition Stands of trees planted at high
densities would capture the site and its resources more rapidly
compared with low-density stands. This would impede the
development of weed communities and result in faster early
tree growth.
(3) Mycorrhizal associations Most forest trees, including
Douglas-fir, form mycorrhizal associations. A dense plantation
might form more rapid connections among tree roots and
mycorrhizal hyphae than a sparse plantation (Perry et al. 1992,
RED:FAR RED SIGNALING AND GROWTH RESPONSE IN DOUGLAS-FIR
Amaranthus and Perry 1994), hence providing more carbon for
the mycorrhizal mat and promoting its growth and vigor. This
would result in greater benefits to the trees and more rapid
early growth.
(4) Root grafting Root grafting would occur sooner in dense
plantings than in sparse plantings. Trees could then share and
exploit site resources more efficiently and early growth would
be enhanced.
(5) Nitrogen mineralization Compared to roots in a sparse
plantation, roots in a dense plantation would exploit the rhizosphere more rapidly and increase the rate of nitrogen mineralization, through root exudates, leading to more rapid early
tree growth.
(6) Perception and avoidance of future competition Trees
growing in close proximity with other trees are able to ‘‘perceive’’ the presence of these future competitors. This is followed by a change in growth programing that focuses on
height growth in order to avoid overshadowing (Aphalo and
Ballaré 1995). The mechanism of perception might be through
R:FR signaling, or by root contact (Mahall and Callaway
1991).
This experiment failed to reject hypothesis No. 6 as it related
to R:FR signaling. However, it did not test whether root interactions, competing brush, or animals have effects on early
height growth in young stands. Further research will be required to determine the significance of these potential effects.
Despite the fact that the Nelder variable density planting was
carried out in miniature in a greenhouse, its results are in
concert with both the field observations of Scott et al. (1992)
and with ‘‘growth waves’’ often observed in full-scale field
Nelder plantings (Figure 6). In the field, increases occurred in
height and stem diameter. In the greenhouse, height, branch
number, and top weight increased, whereas stem diameter did
not. However, if diameters varied across densities in the same
165
proportion as heights (about 10%), then the maximum differences in diameter would have been on the order of only
0.5 mm. It is possible that the hand method used to measure
stem diameter may not have been of sufficient precision to
detect differences at this scale.
Results of both greenhouse and field measurements of R:FR
radiation supported the R:FR signaling hypothesis. In both
cases, R was depleted relative to FR as plant density increased.
Differences in R:FR are perceived by the plant through the
phytochrome system. Evidence from a wide range of plants
species (summarized by Smith 1982, 1994) indicates that stem
extension (height) growth is linearly and negatively related to
phytochrome photoequilibrium (ϕ):
ϕ = Pfr /P,
(1)
where Pfr is the phytochrome fraction in the far-red absorbing
form, and P is the total phytochrome.
To test this with the height data obtained from the greenhouse study, ϕ values were estimated from the R:FR values
measured on August 23 (Figure 5, August 23 values) based on
the relationship provided by Smith (1982, Figure 2). Plant
height, plotted as a function of estimated ϕ, yielded the predicted linear relationship with a strong negative slope (Figure 7) providing further support for the interpretation that the
observed growth response was mediated by phytochrome.
Once the R:FR signal is perceived and transduced, plants
presumably alter their internal growth program in such a manner as to gain greater light harvesting ability in crowded situations (i.e., greater height) and improve their competitive
position. This might occur by increasing the efficiency of
either carbon assimilation or use, or both, or by changing
carbon allocation patterns, or both. The final plant biomass
distributions across the six densities provide insight as to what
Figure 6. An aerial photograph
of two side-by-side, five-yearold Nelder test plots near
Turner, Oregon. At this time,
trees growing near the center
of the plots, at high densities,
were showing considerably
greater height (and diameter)
growth than trees growing in
the outside rows. Over time
these ‘‘growth waves’’ typically move outward. Photograph was taken in 1978,
photographer is unknown.
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RITCHIE
Figure 7. Relationship of Douglas-fir seedling final height to estimated
phytochrome photoequilibria. Numbers in parentheses are arc numbers from the origin of the Nelder fan. Each point is a mean ± 1 SE of
all plants from all fans (about 25 plants per point).
may have occurred in the greenhouse study. Root weights
decreased and total plant weights remained relatively constant,
whereas top weights increased with density, resulting in a
decreasing root:shoot ratio (Figure 4). This suggests that an
increase in carbon allocation to above-ground parts, relative to
below ground parts, may have occurred as a response to the
R:FR signals and altered ϕ. This is consistent with observations on soybean (Glycene max (L.) Merr.) (Kasperbauer
1987), and red beet (Beta vulgaris L.) (Hole et al. 1984).
Other interpretations of these results cannot be ruled out,
however. It is possible, for example, that subtle gradients in
temperature, vapor pressure deficit, air movement, or other
factors could have occurred within the fans and might have
been implicated in the observed growth responses. However,
this does not seem likely for the following reason. Weekly
height measurements begun when the seedlings were just
emerging from the cotyledon stage are shown in Figure 8.
These growth curves show that the seedlings in Arcs 2 (highest
density) and 6 (lowest density) were beginning to differentiate
themselves from those in the other arcs as early as 45 days after
sowing when the seedlings were only about 5.5 cm tall. It
seems unlikely that, at this diminutive size, they could have
modified the environment around seedlings growing 15 cm
away sufficiently to cause them to alter their growth patterns.
Nevertheless, this explanation cannot be discounted without
further experimentation.
If the density effect evident in the field trials is, in fact,
triggered by R:FR signaling among seedlings, it represents a
considerable extension of the reported physical distances
across which such signals are perceived. Field measurements
of R:FR were made at various distances from artificial canopies constructed of tobacco (Nicotiana tobacum L.) or mustard
(Sinapis alba L.) plants with a spectroradiometer equipped
with a cosine corrected sensor (Smith et al. 1990). Red depletion and far-red enhancement were detected at a maximum
Figure 8. Height growth curves for Douglas-fir seedlings from Spokes
‘‘B’’ and ‘‘F’’ in across four fans beginning when seedlings had just
emerged from the cotyledon stage. Plants in Arc 2 are growing at the
highest density, whereas those in Arc 6 are at the lowest density.
distance of 30 cm from these canopies. If R:FR signaling is
triggering the density effect in our plantations, these signals
must be propagated for a distance of at least 6 m, for that is the
distance between seedlings planted at 3,000 trees ha −1. Independent measurements, made with the integrating cylinder
adjacent to a 2.5-m-tall Douglas-fir hedge, showed a measurable R depletion and FR enhancement out to approximately
3 m from the hedge (unpublished data).
A perplexing question that bears on this interpretation involves the role of lesser vegetation. Presumably such plants
would also deplete red light energy, depressing the R:FR
reflected from their foliage and sending ‘‘false signals’’ to the
Douglas-fir seedlings. How would Douglas-fir seedlings discriminate among signals from plants that do not represent
potential competitors and those that do (i.e., other tree species)? Several possible explanations come to mind. First, signal timing may be important. Trees may be sensitive to the
R:FR signal only during early spring, when their shoots are
elongating, but before weeds and deciduous plants are in full
leaf. Five-minute exposure of soybean plants to altered R:FR
was sufficient to induce changes in morphogenesis (Kasperbauer 1987), and elongating shoots are apparently the sites of
R:FR perception in other species (Morgan et al. 1980, Child
and Smith 1987, Ballaré et al. 1990). Alternatively, the phytochrome mechanism may be sufficiently sophisticated to discriminate among the reflectance properties of the leaves
(Woolley 1971, Lee and Graham 1986) of different plants.
Phytochrome is not a single molecular species, but is comprised of a broad family of photoreceptors encoded by multiple
divergent genes (Quail 1994). To complicate matters further,
the ability of some plants to respond to phytochrome is dependent on the presence of blue or ultraviolet (UV-A) light
(Mohr 1994). Such ‘‘coaction’’ between plant pigment systems
has been demonstrated in Scots pine seedlings by Fernbach
and Mohr (1990). Such richness of information-gathering
RED:FAR RED SIGNALING AND GROWTH RESPONSE IN DOUGLAS-FIR
leads to speculation that not only detection, but identification,
of neighboring plants might be occurring in nature.
From a practical standpoint, the growth promoting effects of
R:FR signaling can be exploited in forest management by
increasing planting density and developing early thinning and
silvicultural prescriptions to maintain proper stocking densities. This is now being done in certain areas of the coastal
Pacific Northwest. It is doubtful that greenhouse or nursery
production could be enhanced, however, because typical growing densities are already capturing the density effect.
The implications of this phenomenon to modeling competition in forest stands are obvious. The incorporation into such
models, of algorithms simulating sophisticated informationgathering systems (Aphalo and Ballaré 1995) such as R:FR
signaling, would tend to enhance their predictive ability beyond that of models based solely on passive plant responses to
resource limitations. This could lead to fundamentally new
ways of thinking about the biology of plant competition and
interaction, and should stimulate a great deal of additional
research.
Acknowledgments
The capable technical assistance of James Keeley and Patty Ward is
gratefully acknowledged. I also appreciate the generous cooperation
of the Weyerhaeuser Company Rochester Regeneration Center staff in
growing plants and for providing space to conduct this study. I thank
Dr. Carlos Ballaré, University of Buenos Aires, Argentina for advice
and for providing a prototype of the integrating cylinder used in the
spectroradiometric measurements. Weyerhaeuser colleagues Drs.
Wm. Scott, Roger Timmis, Christine Dean, Wm. Carlson, and Peter
Farnum, along with Steven Duke and Paul Figueroa reviewed earlier
drafts of this paper. Drs. R. van den Driessche, R. Guy, C. Harrington,
T. Terry and R. Edmonds contributed to hypothesis development. Prof.
Harry Smith, Univ. of Leicester, UK, and two anonymous referees
provided reviews of the submission manuscript. A special thank you
to Dr. Barbara Yoder, Oregon State University, who planted the early
ideas for this work and provided me with two seminal papers on the
topic of R:FR signaling. This research and its publication were supported by Weyerhaeuser Company.
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