Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol15.1995:
Tree Physiology 15, 307--315
© 1995 Heron Publishing----Victoria, Canada
Effects of light availability and tree size on the architecture of
assimilative surface in the canopy of Picea abies: variation in needle
morphology
ÜLO NIINEMETS1,2 and OLEVI KULL1
1
Institute of Ecology, Estonian Academy of Sciences, 40 Lai Str., EE 2400 Tartu, Estonia
2
Present address: LS Pflanzenökologie, BITÖK, Universität Bayreuth, Postfach 10 12 51, 95448 Bayreuth, Germany
Received July 10, 1994
Summary Needle dimensions, needle surface area, needle
dry weight per area (LWA) and needle density (ND, needle
weight per volume) were measured in terminal current-year
shoots in a natural canopy of variably sized Picea abies (L.)
Karst. trees growing along a light gradient. Needle shape was
described as a rhomboid. Needle width (D2) increased with
increasing diffuse site factor, ad (relative amount of penetrating
diffuse solar radiation), whereas needle thickness (D1) remained nearly constant, resulting in an inverse relationship
between D1/D2 and ad and an increase in the ratio of total (TLA)
to projected needle surface area (PLA) with increasing ad.
Because of the variations in needle morphology with respect
to light availability, the shoot parameters used in present canopy models are also expected to be light-sensitive, and studies
involving shoot morphology should also consider the variability in needle geometry. Needle dimensions and total tree height
were not correlated. However, LWA increased with both increasing ad and total tree height. When LWA was expressed as
the product of ND and needle height (NH, height of the
rhomboidal transverse section of a needle), LWA appeared to
increase with irradiance, because of changing NH, and with
total tree height, because of changing needle density.
Keywords: conifers, leaf area estimation, leaf area index, leaf
density, leaf morphology, leaf thickness, leaf weight per area,
Norway spruce, tree dimensions.
Introduction
Estimates of leaf area index (LAIp, projected leaf surface area
per ground area) are often used to derive total leaf surface area
index (LAIt). With broad-leaved species, a simple conversion
factor of two is employed to calculate LAIt from LAIp, because
leaf surface area is not influenced significantly by leaf thickness. However, in coniferous species with needle-shaped
leaves, total needle surface area is a function of needle thickness (Witkowski and Lamont 1991). To further complicate
matters, environmental factors also affect needle morphology
(Tucker and Emmingham 1977, Greis and Kellomäki 1981,
Jordan and Smith 1993). Consequently, estimates of the sur-
face area of assimilative organs of coniferous species are not
possible without considering the developmental responses of
needle morphology to local microclimate conditions.
Recent models of conifer photosynthesis examining the
influence of shoot structure on photosynthetic production
(e.g., Oker-Blom 1985, Wang and Jarvis 1993) are based on the
assumption that needle structure is constant throughout the
tree. However, Jordan and Smith (1993) have shown that
variation in needle geometry can result in variation in photosynthetic rates as a result of changes in the surface area for
interception of light. Thus, estimates of light interception by
shoots may be improved if the environmental factors responsible for variation in needle structure are identified, and needle
geometry is characterized.
Although qualitative differences in foliage properties with
respect to long-term changes in light availability have been
examined in broad-leaved species (e.g., Lichtenthaler 1985),
little is known about how spatial variation in needle morphology is related to canopy light gradients. In general, rates of
physiological processes are higher in trees in sunny than in
shady habitats, especially when calculated on a foliage area
basis (Björkman 1981), because sun trees access more solar
energy, which speeds up light-dependent metabolic reactions,
and foliar structure is adapted to the prevailing light conditions
so that the capacity for light utilization is dependent on the
growth radiation regime (Prioul and Bourdu 1973, Björkman
1981). Because leaf dry weight per area (LWA) increases
linearly (Gulmon and Chu 1981, Jurik 1986, Oren et al. 1986,
ermák 1989, Kull and Niinemets 1993) and its reciprocal,
specific leaf area (SLA), decreases hyperbolically (Drew and
Ferrell 1977, Tucker and Emmingham 1977, Del Rio and Berg
1979, Kellomäki and Oker-Blom 1981, Koppel and Frey 1984,
van Hees and Bartelink 1993) with irradiance during leaf
growth, they are frequently used to characterize effects of light
on leaf structure. Moreover, there is often a strong positive
correlation between LWA and leaf photosynthetic capacity
(light-saturated photosynthesis) per area (Björkman 1981, Jurik 1986, Oren et al. 1986), which has been interpreted as
evidence that plant resources are invested where photosynthetic returns are highest (Gutschick and Wiegel 1988). Thus,
308
NIINEMETS AND KULL
variation in LWA with light is adaptive. However, in addition
to variation with irradiance, LWA correlates with plant age and
dimensions (Hager and Sterba 1985, Linder 1985, Chazdon
1986, Steele et al. 1989, Leuning et al. 1991, Kull and Niinemets 1993), leaf aging and development (Del Rio and Berg
1979, Hager and Sterba 1985, Oren et al. 1986, Wang et al.
1990), season (Lewandowska and Jarvis 1977, Smith et al.
1981, Reich et al. 1991), water availability (Rascio et al. 1990),
altitude (Körner et al. 1986), and nutrient availability (Araki
1971, Dijkstra 1990, Witkowski and Lamont 1991). In an
attempt to partition the variation in LWA between different
environmental factors, Witkowski and Lamont (1991) defined
LWA as the product of leaf density (dry weight per volume)
and thickness (LWA = density × thickness). Although the
factors affecting LWA may influence each of these variables,
density and thickness often respond independently (Witkowski
and Lamont 1991). Consequently, partitioning the variation in
LWA between its components can be more useful than the
examination of LWA--environment relationships only. To understand better the dependence of LWA and other needle characteristics on environmental factors, we examined needle
morphology in relation to light climate and total tree height in
a Picea abies (L.) Karst. canopy.
Material and methods
The study was performed in the nemoral spruce forest at Voore
Ecological Station, Estonia (58°44′ N, 26°45′ E, elevation
90 m above sea level), at the beginning of August 1989. The
forest is located on a plateau-like crest of a drumlin with brown
pseudopodzolic soil. A detailed description of the study site is
given by Frey (1977).
Current-year shoots at terminal positions were taken from
the southern aspect of six trees with variable exposure. Total
height of sampled trees ranged from 1.60 to 35.5 m, whereas
tree age was estimated to range from 8 to 105 years. Every
sample consisted of four to seven shoots. To ensure sampling
along the vertical light gradient, shoots were collected at three
to five different canopy heights per tree. Sample and total tree
heights were also measured. The highest relative sampling
height (sampling height per total tree height) per tree ranged
from 0.78 to 0.96. Means were calculated for all parameters
from all sampled shoots per sampling location.
Relative irradiances in the sampling locations were estimated by a hemispherical (‘‘fish-eye’’) photographic technique
(Anderson 1964) as modified by Nilson and Ross (1979).
Several photographs were taken per sampling location, and
from every photograph, the proportion of canopy gaps was
measured with respect to zenith angle. The diffuse site factor,
ad (relative amount of penetrating diffuse solar radiation), was
calculated as the mean for all photographs from a sampling
location: ad = 1.0 corresponds to the diffuse irradiance above
the stand, and ad = 0.0 to complete shade with no canopy gaps.
Estimated this way, ad provides comparable estimates to other
light sensors, especially if long-term variation in irradiance is
of interest (Salminen et al. 1983). Because the sampling locations were always on the southern aspect, no correction for
differences in direct solar radiation associated with sample
compass direction was necessary.
Total tree height, a second independent variable, was hypothesized to cause changes in foliage structure as a result of
changes in tree water balance and stronger gradients of environmental factors in the crowns of taller trees.
Ten needles from the central part of a shoot were randomly
taken for the measurement of total needle area (TLA) (Frey
1981, Steele et al. 1989). Needle thickness (D1), width (D2) in
the center of each needle, and needle length (Ln) were measured with a micrometer, and the total surface area was calculated by the formula of Ivanov (Gulidova 1959, Figure 1):
TLA = 2Ln√
D21 + D
22 .
(1)
Equation 1 describes the needle shape as a rhomboid. The
variables D1 and D2 are given in anatomical terms, i.e., upper
and lower surface, and accordingly, thickness and width of a
leaf are determined by the disposition of leaf xylem and
phloem. In P. abies, needle thickness (1.15--1.5 mm) is usually
larger and less variable than needle width (0.4--1.5 mm)
(Aussenac 1973, Frey 1981), and the needles are oriented in
space so that the mean angle between the largest projections
and the horizon is less for D1 than for D2. Therefore, needle
thickness and width, defined in this way, are homologous to
leaf width and thickness of broad-leaved species, respectively.
One measure of projected needle surface area (PLA) was
calculated as:
PLA 1 = Ln (Ld + z ),
(2)
where Ld is needle side length, and Ld + z is equal to projected
D1 (Figure 1). Assuming D1 > D2, and substituting
z=
Ld =
D21 − D22
2√
D 21 + D
22
√
D21 + D
22
2
and
gives
Figure 1. Geometrical model of a needle: D1 = needle thickness, D2 =
needle anatomical width, Ld = side length, NH = needle height, and
Ld + z = projected needle thickness.
IRRADIANCE AND TREE SIZE ON NEEDLE MORPHOLOGY
D21
PLA1 = Ln 2
.
2
D1 + D
2
√
(3)
Another measure for PLA was calculated as:
PLA 2 = Ln D1.
needles at 85 °C for 48 h, and needle dry weight per TLA and
PLA1 (LWAt and LWAp, respectively), and needle density (ND)
were calculated. Because LWAt is the product of leaf density
and thickness (Witkowski and Lamont 1991), or for P. abies,
of ND and needle height (NH, projection of needle width,
Figure 1), it can be computed as:
(4)
The value of PLA2 is always larger than the value of PLA1. The
geometric estimate, PLA1, was considered to be closer to the
PLA in the natural needle position on a shoot and was therefore
used in our study (except as noted). Nevertheless, no qualitative differences in relationships occurred when Equation 4 was
used instead of Equation 3. Steele et al. (1989) found that
measurements made with a photoelectric planimeter significantly underestimated PLA in Picea sitchensis (Bong.) Carr.
when compared to a geometric model. Accordingly, we expected PLA, measured directly by a video device or photoelectric planimeter, for needles spread on a flat surface to be in
between the geometric estimates PLA2 and PLA1, because
needles are often curved or twisted in shape. Furthermore, as
D2 or D1 change, probabilities for arranging the needles on D1
or on projected D1 and consequently, measuring PLA in the
direction of Ld + z or D1 also change. To test this assumption,
calculations based on Equations 3 and 4 were compared to
estimates of PLA measured with a video areameter (DIAS,
Delta-T Devices, Cambridge, U.K.) that was previously calibrated as described by Diebolt and Mudge (1988). On average,
Equation 3 underestimated projected needle area (PLAm) by
9.5%, and Equation 4 overestimated PLAm by 13% (Figure 2),
indicating that PLA measurements were sensitive to the variability in needle morphology.
Needle volume (V) was calculated as:
D1 D2
V = Ln
.
2
309
(5)
Needle weight (Mn) was determined after oven-drying the
LWAt =
Mn
V
= ND
,
TLA
TLA
where
(6)
D 1 D2
V
NH
=
=
.
TLA 4√
4
D21 + D
22
(7)
Often, shoot structure is characterized by the ratio of shoot
silhouette area to total needle surface area (STAR), where
shoot silhouette area is defined as the total shadow cast by a
shoot when the radiation beam is perpendicular to the shoot
axis (e.g., Boyce 1993). Assuming that all needles lie in the
same plane, side by side, then the possible maximum value,
STARcal, can be calculated when needle number per shoot (N),
shoot length (Ls), needle thickness (D1), PLA and TLA are
known:
STARcal =
PLA 2
,
TLA × SF
(8)
where SF is a factor accounting for possible space limitations
due to the variation in needle number per shoot length. If
D1N/(2Ls) > 1, there are more needles per shoot than can be
accommodated according to the definition of STARcal, resulting in needle overlap and shading between needles, and SF =
D1N/(2Ls). However, if D1N/(2Ls) ≤ 1, all needles can theoretically be placed in the same plane, side by side, and SF = 1. The
variable PLA2 is used because the maximum value of STARcal
is of interest.
Linear correlation and regression techniques were used to
analyze the data. Statistical relationships were considered significant if P < 0.05. All abbreviations and respective units are
listed in Appendix 1.
Results
Total tree height and ad were not correlated (P > 0.2). Relative
sampling height (Rh) was significantly correlated with light
availability (P < 0.001), and ad decreased nonlinearly with
decreasing Rh. Total tree height and Rh were not significantly
related. Thus, the effects of total tree height and ad on needle
structure could be studied independently.
Figure 2. Comparison between projected needle surface area measured
by a video areameter, PLAm (mm2), and PLAc (mm2) calculated from
measured needle parameters using Equations 3 (PLA1, d) and 4
(PLA2, s): PLAm = 1.02PLA1 + 1.00 (r2 = 0.934, P < 0.001, n = 36),
and PLAm = 0.89PLA2 − 0.38 (r2 = 0.958, P < 0.001, n = 36). For both
regression equations, the intercept did not differ significantly from
zero.
Needle dimensions and surface area
Needle thickness was not significantly related to irradiance
(Figure 3A). In contrast, needle width increased significantly
with ad (P < 0.00001, Figure 3B). As a result, D1/D2 decreased
(Figure 3C) and TLA/PLA increased (Figure 3D) linearly as
irradiance increased (P < 0.00001).
310
NIINEMETS AND KULL
Figure 3. Effects of relative irradiance (ad) on needle dimensions
and surface area. (A) Needle
thickness (D1, mm) versus ad: D1
= 0.17ad + 1.06 (r2 = 0.085, P >
0.2, n = 18). (B) Needle anatomical width (D2, mm) versus ad: D2
= 0.68ad + 0.46 (r2 = 0.730, P <
0.00001, n = 18). (C) D1/D2 versus ad: D1/D2 = −1.11ad + 2.05 (r2
= 0.829, P < 0.00001, n = 18).
(D) Total leaf area to projected
leaf area ratio (TLA/PLA) versus
ad: TLA/PLA = 2.40 + 1.06ad (r2
= 0.719, P < 0.00001, n = 18).
There was a tendency for PLA1/PLAm (Figure 2) to decrease
with D1/D2 (PLA1/PLAm = 1.34 − 0.19D1/D2, r2 = 0.315, P <
0.001, n = 36), and PLA2/PLAm to increase with D1/D2
(PLA2/PLAm = 0.76 + 0.08D1/D2, r2 = 0.127, P < 0.05, n = 36).
Consequently, with respect to measured PLA, underestimation
of PLA1 increased with decreasing D1/D2 (higher ad), and
overestimation of PLA2 increased at higher D1/D2 values
(lower ad) compared with measurements made with a video
areameter.
Total and projected needle surface areas (TLA and PLA) and
needle length were not significantly related to irradiance. No
correlations were found between total tree height and measured needle dimensions. There was a tendency for needle
length to increase with total tree height, but this was not
significant at P < 0.05.
The ratio of computed shoot silhouette area to total needle
surface area (STARcal) decreased significantly with increasing
ad (Figure 4). Tree height did not influence STARcal.The quantity D1N/(2Ls) (Equation 8) increased with increasing light and
tree height (r2 = 0.748, P < 0.0001).
Needle weight per area, volume, density and height
Needle volume and surface area of needle transverse sections
(0.5D1 × D2) were significantly correlated with ad (r2 = 0.272
and 0.315, respectively, P < 0.05). Needle dry weight per total
surface area (LWAt) and per projected surface area (LWAp)
increased with increasing ad and tree height (P < 0.00001,
Figures 5A and 5B). The value of LWAp, equal to
TLA
LWAp = LWAt
,
PLA
(9)
was more strongly related to ad than LWAt as a result of the
relationship between TLA/PLA and ad.
Variation in LWA with increasing total tree height and ad was
examined in more detail by considering the components of
LWA, needle density and needle height (Equations 6 and 7).
Needle density increased with total tree height (P < 0.00001,
Figure 6A) but was not correlated with ad (Figure 6B). The
ratio of needle volume to TLA (Equation 7) was linearly
related to ad (P < 0.00001, Figure 6D), but it was independent
of total tree height (Figure 6C). Both LWAt and LWAp were
correlated positively with NH and ND. Thus, the dependence
of LWA on ad can be attributed to changes in needle height,
whereas increases in LWA with total tree height can be attributed to increasing needle density. The correlation between
needle height and density was not significant (r2 = 0.009, P >
0.95).
Discussion
Needle dimensions and surface area
Figure 4. Calculated (Equation 8) shoot silhouette area to total needle
surface area ratio (STARcal) versus ad. The value of STARcal combines
the changes in projected to total leaf area ratio and needle number per
unit shoot length. STARcal = −0.174ad + 0.456 (r2 = 0.529, P < 0.001,
n = 17).
Because of the complex nature of needle geometry in P. abies
(e.g., Kerner et al. 1977), needle morphology was only approximated by a rhomboid. Frey (1981) evaluated many geometrical formulas for P. abies and found that the rhomboidal
model (Equation 1) gave the most reliable estimates of TLA
IRRADIANCE AND TREE SIZE ON NEEDLE MORPHOLOGY
311
Figure 5. Needle dry weight per
area in relation to total tree height
(m) and ad. (A) Needle weight per
TLA (LWAt, g m −2): LWAt =
0.635(tree height) + 29.7ad + 35.8
(r2 = 0.829, P < 0.00001, n = 17).
(B) Needle weight per PLA
(LWAp, g m − 2, Equation 9):
LWAp = 1.79(tree height) +
157ad + 75.0 (r2 = 0.874, P <
0.00001, n = 17).
Figure 6. Effects of total tree
height (m) and ad on needle density (ND, g cm −3) and needle volume per TLA (V/TLA, mm3
mm −2). (A) ND versus total tree
height: ND = 0.0035(tree height)
+ 0.33 (r2 = 0.761, P < 0.00001,
n = 17). (B) ND versus ad: ND =
0.021ad + 0.381 (r2 = 0.006, P >
0.8, n = 17). (C) V/TLA versus
tree height: V/TLA = 0.00066(tree
height) + 0.136 (r2 = 0.110, P >
0.2, n = 18). (D) V/TLA versus
ad: V/TLA = 0.107ad + 0.110 (r2
= 0.605, P < 0.001, n = 18).
over a wide range of D1/D2 ratios. However, compared to TLA
calculated as the product of needle perimeter and length,
Ivanov’s formula (Equation 1) underestimated TLA by a factor
of 0.94 in Picea rubens Sarg. (Boyce 1993) and 0.92--0.95 in
P. abies (Frey 1981), because the real needle perimeter was
longer than that predicted from the rhomboidal model. Nevertheless, precise estimation of TLA was not critical for the
qualitative relationships presented here, because the error due
to underestimated TLA was less than the variation due to total
tree height and ad. Moreover, because PLA, measured for
detached needles laid out on a flat surface varies systematically
with changing D1/D2, estimation of projected area based on a
geometrical model may be more explicit.
There is, at least up to a certain age, a strong relationship
between height and age of woody plants, thus tree height could
serve as an estimate of tree age. Although needle parameters,
except for needle weight per area and needle density, were not
dependent on total tree height, many needle morphological
traits correlate with tree age, e.g., SLA, D1, TLA and Mn in
P. sitchensis (Steele 1984, Steele et al. 1989) and Pinus radiata
D. Don (M. Steele, personal communication). Variation in
needle morphology with age in P. sitchensis was nonlinear,
whereas needle structure changed more rapidly in younger
plants (1 to 10 years old) than in older plants (over 10 years
old). Large spatial extensions and the long life spans of trees
make it difficult to study the effects of light availability and
tree age on foliage structure independently in the same stand,
but with grafted conifer scions placed in approximately the
same irradiance, variations in several needle parameters, e.g.,
Ln and Mn in Pinus taeda L. (Greenwood 1984), and Ln in Larix
laricina (Du Roi) K. Koch (Greenwood et al. 1989), were
related only to scion age. Thus, our a priori assumption that
variation in total tree height and associated changes in water
relations are the mechanistic reason for variation in needle
parameters with tree age may not be fully justified.
Leverenz and Jarvis (1980) reported that sun needles of
P. sitchensis had greater D1 and PLA than shade needles. No
relationships between ad and needle surface area (PLA and
TLA) or D1 were found in our study, whereas D2 was significantly correlated with ad. Because pronounced gradients of
light and needle development exist within a conifer shoot, the
morphological parameters vary considerably (Frey 1981, Frey
and Ivask 1983, Chandler and Dale 1990, Brewer et al. 1992,
Powell 1992), and 10 randomly taken needles per shoot may
not be sufficient to detect all structural differences caused by
the light environment. However, Brewer et al. (1992) reported
312
NIINEMETS AND KULL
that, in Abies fraseri (Pursh) Poir., D1 and D2 were relatively
constant at different positions within the shoot. Furthermore,
Powell (1992) found that in Tsuga canadensis (L.) Carr.,
several structural parameters of needles were related to shoot
length, which characterizes shoot vigor rather than light availability. Accordingly, one might conclude that several modifications in needle morphology may in fact be unrelated to
irradiance.
Koch (1976) reported that D2/D1 is dependent on irradiance,
and a quasi-linear relationship between D1/D2 and relative
irradiance, as was found in our study, has been found previously in P. abies (Aussenac 1973, Greis and Kellomäki
1981). Similarly, Jordan and Smith (1993) reported that needle
thickness was significantly lower in shade leaves than in sun
leaves of Abies lasiocarpa (Hook.) Nutt., and the ratio of
needle thickness to width was greater for sun needles, corresponding to our results (Figures 3B and 3C) (cf. Material and
methods). Recalculation of the data reported by Aussenac
(1973) for Abies nordmanniana (Steven) Spach. and Pseudotsuga menziesii (Mirb.) Franco resulted in a similar relationship. A constant value for TLA/PLA has been used to calculate
TLA or PLA in conifers when only one of them is measured.
Values reported include 2.429 for Abies balsamea (L.) Mill.
(Boyce 1993), 2.26 for Abies concolor (Gord.) Lindl. ex
Hildebr., 2.41 for Abies magnifica A. Murr. (Westman 1987),
2.57 for Pinus sylvestris L. (Roberts et al. 1982), 2.714 for
P. rubens (Boyce 1993), and 2.5 (Oren et al. 1986), 2.6 (Zimmermann 1990), 2.61 (Münster-Swendsen 1987) and 2.74
(Riederer et al. 1988) for P. abies. However, because of the
relationship between D1/D2 and irradiance, the ratio of total to
projected needle area also changes with light conditions in the
canopy. Consequently, TLA may be substantially underestimated in the upper canopy and overestimated in the lower
canopy when calculated based on a constant ratio of
TLA/PLA. Furthermore, changing patterns of TLA/PLA with
irradiance implies that the shoot silhouette area to total needle
area ratio (STAR), a parameter often used exclusively to characterize shoot structure, is likely to vary with needle morphology and ad (Figure 4). However, changes in STAR, resulting
from changing PLA/TLA of needles, can be influenced by
variation in the distribution of needles on a shoot (Niinemets
and Kull, unpublished results), e.g., increases in D1N/(2Ls)
with increasing ad results in decreasing STARcal with increasing ad even if TLA/PLA is constant.
There are methodological problems associated with the use
of different quantities in calculating physiological parameters
(Verduin 1959, Charles-Edwards and Ludwig 1975, Öquist et
al. 1982, ermák 1989, Smith et al. 1991, Jordan and Smith
1993). For example, photosynthetic capacity per needle dry
weight is equal to (photosynthetic capacity per needle
area)/LWA. The value of LWAp contains variations both in
TLA/PLA and LWAt (Equation 9). Additionally, the rates of
physiological processes based on different denominators, e.g.,
PLA, TLA, V and Mn, are not readily comparable when respective irradiances are not known. Moreover, when different species are compared, interspecific differences in needle morphology versus light relationships may need to be considered.
Needle weight per area, volume, density and height
The independent components of LWAt, needle height and
needle density, showed qualitatively different behavior with
respect to total tree height and irradiance. An increase in needle
height (projected needle width, D2) with ad is comparable to an
increase in leaf thickness with light in broad-leaved species,
thus characterizing the effect of light on cell size and division
(Jackson 1967, Nobel 1977, Nobel and Hartsock 1981,
Malkina 1983, Nygren and Kellomäki 1983). Because of the
dependence of needle height on light, other parameters, e.g., V
and the area of a needle transverse section (Figures 3B and
6D), were also correlated with ad. Similarly, in Picea schrenkiana Fisch. et C.A. Mey., needles from the southern aspect
(higher irradiance) had more and larger mesophyll cells, resulting in a significantly higher needle transverse section area
(Baidavletova 1984), than those from the northern aspect
(lower irradiance). Frey (1981) reported that sun needles of
P. abies have six to eight layers of mesophyll cells and shade
needles two to three layers in the direction of needle width
(D2), whereas for D1, the number of cell layers was similar
(seven to nine). Thus, the increase in needle height and V/TLA
with increasing irradiance could be attributed to a change in
needle width (D2). In an ecological context, enhanced leaf
thickness may be advantageous, resulting in an increase in leaf
mesophyll area per surface area and consequently, increasing
the diffusive conductance of the mesophyll to CO2 (Nobel
1977). Moreover, greater light absorptance, due to increasing
path length, is expected in thick leaves compared to thin leaves
(Öquist et al. 1982).
Variation in leaf density can be attributed to differences in
chemical composition and anatomical structure of leaves (accumulation of metabolites such as starch, differences in composition and thickness of cuticle and cell walls, cell size, and
frequency and size of intercellular spaces) (Rascio et al. 1990,
Witkowski and Lamont 1991). The significance of increasing
needle density with total tree height is not easily explained.
Accumulation of certain metabolites could indicate decreased
sink capacities for photosynthate utilization as growth rates
decrease with increasing tree age. On the other hand, as environmental stresses increase with total tree height, it may be
necessary to build needles that are increasingly resistant, i.e.,
have less intercellular spaces, a thicker cuticle and thick cell
walls. Indeed, indirect data show that the actual amount of
photosynthesizing tissue per unit leaf weight decreases with
increasing tree age or height. Older P. abies trees grown in
open areas have lower TLA- and weight-based photosynthetic
capacities than younger trees (Kull and Koppel 1987). It appears that needles, with the same area for light interception and
gaseous exchange, have higher carbon cost in taller and older
trees because needle density and LWA increase. Kull and
Niinemets (1993) proposed that the carbon requirement for
supporting tissues is larger in crowns of tall trees than in
crowns of small trees because of the need to survive water
deficits and lower water potentials. Although the change in
water potential due to gravitational force is only about 0.01
MPa m −1, gradients of water potential between 0.1 and 0.2
MPa m −1 have been reported in stems of P. sitchensis
IRRADIANCE AND TREE SIZE ON NEEDLE MORPHOLOGY
(Hellkvist et al. 1974). These gradients may be sufficiently
large to cause differences in needle morphology.
Acknowledgments
Dr. Ron J. Ryel (Dept. Range Science, Utah State University, USA)
and Prof. Dr. John D. Tenhunen (LS Pflanzenökologie, BITÖK, Universität Bayreuth, Germany) are gratefully acknowledged for their
invaluable comments on earlier drafts of this manuscript.
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IRRADIANCE AND TREE SIZE ON NEEDLE MORPHOLOGY
Appendix 1. Abbreviations and units.
Abbreviation
Definition
Unit
ad
D1
D2
Ld
Ld + z
Ln
Ls
LWAt
LWAp
Mn
SF
N
ND
NH
PLA
PLAc
PLA1
PLA2
PLAm
Rh
TLA
V
STARcal
Diffuse site factor
Needle thickness
mm
Needle width
mm
Needle side length
mm
Projected D1
mm
Needle length
mm
Shoot length
mm
Mn per TLA
g m −2
Mn per PLA1
g m −2
Needle dry weight
µg
Factor of needle spacing
Needle number per shoot
Needle density
g cm −3
Needle height (projected D2)
mm
Projected needle surface area
mm2
Calculated PLA (PLA1, PLA2)
mm2
PLAc (Equation 3)
mm2
PLAc (Equation 4)
mm2
Measured PLA
mm2
Relative sampling height
Total needle surface area
mm2
Needle volume
mm3
Calculated shoot silhouette area to TLA ratio
315
© 1995 Heron Publishing----Victoria, Canada
Effects of light availability and tree size on the architecture of
assimilative surface in the canopy of Picea abies: variation in needle
morphology
ÜLO NIINEMETS1,2 and OLEVI KULL1
1
Institute of Ecology, Estonian Academy of Sciences, 40 Lai Str., EE 2400 Tartu, Estonia
2
Present address: LS Pflanzenökologie, BITÖK, Universität Bayreuth, Postfach 10 12 51, 95448 Bayreuth, Germany
Received July 10, 1994
Summary Needle dimensions, needle surface area, needle
dry weight per area (LWA) and needle density (ND, needle
weight per volume) were measured in terminal current-year
shoots in a natural canopy of variably sized Picea abies (L.)
Karst. trees growing along a light gradient. Needle shape was
described as a rhomboid. Needle width (D2) increased with
increasing diffuse site factor, ad (relative amount of penetrating
diffuse solar radiation), whereas needle thickness (D1) remained nearly constant, resulting in an inverse relationship
between D1/D2 and ad and an increase in the ratio of total (TLA)
to projected needle surface area (PLA) with increasing ad.
Because of the variations in needle morphology with respect
to light availability, the shoot parameters used in present canopy models are also expected to be light-sensitive, and studies
involving shoot morphology should also consider the variability in needle geometry. Needle dimensions and total tree height
were not correlated. However, LWA increased with both increasing ad and total tree height. When LWA was expressed as
the product of ND and needle height (NH, height of the
rhomboidal transverse section of a needle), LWA appeared to
increase with irradiance, because of changing NH, and with
total tree height, because of changing needle density.
Keywords: conifers, leaf area estimation, leaf area index, leaf
density, leaf morphology, leaf thickness, leaf weight per area,
Norway spruce, tree dimensions.
Introduction
Estimates of leaf area index (LAIp, projected leaf surface area
per ground area) are often used to derive total leaf surface area
index (LAIt). With broad-leaved species, a simple conversion
factor of two is employed to calculate LAIt from LAIp, because
leaf surface area is not influenced significantly by leaf thickness. However, in coniferous species with needle-shaped
leaves, total needle surface area is a function of needle thickness (Witkowski and Lamont 1991). To further complicate
matters, environmental factors also affect needle morphology
(Tucker and Emmingham 1977, Greis and Kellomäki 1981,
Jordan and Smith 1993). Consequently, estimates of the sur-
face area of assimilative organs of coniferous species are not
possible without considering the developmental responses of
needle morphology to local microclimate conditions.
Recent models of conifer photosynthesis examining the
influence of shoot structure on photosynthetic production
(e.g., Oker-Blom 1985, Wang and Jarvis 1993) are based on the
assumption that needle structure is constant throughout the
tree. However, Jordan and Smith (1993) have shown that
variation in needle geometry can result in variation in photosynthetic rates as a result of changes in the surface area for
interception of light. Thus, estimates of light interception by
shoots may be improved if the environmental factors responsible for variation in needle structure are identified, and needle
geometry is characterized.
Although qualitative differences in foliage properties with
respect to long-term changes in light availability have been
examined in broad-leaved species (e.g., Lichtenthaler 1985),
little is known about how spatial variation in needle morphology is related to canopy light gradients. In general, rates of
physiological processes are higher in trees in sunny than in
shady habitats, especially when calculated on a foliage area
basis (Björkman 1981), because sun trees access more solar
energy, which speeds up light-dependent metabolic reactions,
and foliar structure is adapted to the prevailing light conditions
so that the capacity for light utilization is dependent on the
growth radiation regime (Prioul and Bourdu 1973, Björkman
1981). Because leaf dry weight per area (LWA) increases
linearly (Gulmon and Chu 1981, Jurik 1986, Oren et al. 1986,
ermák 1989, Kull and Niinemets 1993) and its reciprocal,
specific leaf area (SLA), decreases hyperbolically (Drew and
Ferrell 1977, Tucker and Emmingham 1977, Del Rio and Berg
1979, Kellomäki and Oker-Blom 1981, Koppel and Frey 1984,
van Hees and Bartelink 1993) with irradiance during leaf
growth, they are frequently used to characterize effects of light
on leaf structure. Moreover, there is often a strong positive
correlation between LWA and leaf photosynthetic capacity
(light-saturated photosynthesis) per area (Björkman 1981, Jurik 1986, Oren et al. 1986), which has been interpreted as
evidence that plant resources are invested where photosynthetic returns are highest (Gutschick and Wiegel 1988). Thus,
308
NIINEMETS AND KULL
variation in LWA with light is adaptive. However, in addition
to variation with irradiance, LWA correlates with plant age and
dimensions (Hager and Sterba 1985, Linder 1985, Chazdon
1986, Steele et al. 1989, Leuning et al. 1991, Kull and Niinemets 1993), leaf aging and development (Del Rio and Berg
1979, Hager and Sterba 1985, Oren et al. 1986, Wang et al.
1990), season (Lewandowska and Jarvis 1977, Smith et al.
1981, Reich et al. 1991), water availability (Rascio et al. 1990),
altitude (Körner et al. 1986), and nutrient availability (Araki
1971, Dijkstra 1990, Witkowski and Lamont 1991). In an
attempt to partition the variation in LWA between different
environmental factors, Witkowski and Lamont (1991) defined
LWA as the product of leaf density (dry weight per volume)
and thickness (LWA = density × thickness). Although the
factors affecting LWA may influence each of these variables,
density and thickness often respond independently (Witkowski
and Lamont 1991). Consequently, partitioning the variation in
LWA between its components can be more useful than the
examination of LWA--environment relationships only. To understand better the dependence of LWA and other needle characteristics on environmental factors, we examined needle
morphology in relation to light climate and total tree height in
a Picea abies (L.) Karst. canopy.
Material and methods
The study was performed in the nemoral spruce forest at Voore
Ecological Station, Estonia (58°44′ N, 26°45′ E, elevation
90 m above sea level), at the beginning of August 1989. The
forest is located on a plateau-like crest of a drumlin with brown
pseudopodzolic soil. A detailed description of the study site is
given by Frey (1977).
Current-year shoots at terminal positions were taken from
the southern aspect of six trees with variable exposure. Total
height of sampled trees ranged from 1.60 to 35.5 m, whereas
tree age was estimated to range from 8 to 105 years. Every
sample consisted of four to seven shoots. To ensure sampling
along the vertical light gradient, shoots were collected at three
to five different canopy heights per tree. Sample and total tree
heights were also measured. The highest relative sampling
height (sampling height per total tree height) per tree ranged
from 0.78 to 0.96. Means were calculated for all parameters
from all sampled shoots per sampling location.
Relative irradiances in the sampling locations were estimated by a hemispherical (‘‘fish-eye’’) photographic technique
(Anderson 1964) as modified by Nilson and Ross (1979).
Several photographs were taken per sampling location, and
from every photograph, the proportion of canopy gaps was
measured with respect to zenith angle. The diffuse site factor,
ad (relative amount of penetrating diffuse solar radiation), was
calculated as the mean for all photographs from a sampling
location: ad = 1.0 corresponds to the diffuse irradiance above
the stand, and ad = 0.0 to complete shade with no canopy gaps.
Estimated this way, ad provides comparable estimates to other
light sensors, especially if long-term variation in irradiance is
of interest (Salminen et al. 1983). Because the sampling locations were always on the southern aspect, no correction for
differences in direct solar radiation associated with sample
compass direction was necessary.
Total tree height, a second independent variable, was hypothesized to cause changes in foliage structure as a result of
changes in tree water balance and stronger gradients of environmental factors in the crowns of taller trees.
Ten needles from the central part of a shoot were randomly
taken for the measurement of total needle area (TLA) (Frey
1981, Steele et al. 1989). Needle thickness (D1), width (D2) in
the center of each needle, and needle length (Ln) were measured with a micrometer, and the total surface area was calculated by the formula of Ivanov (Gulidova 1959, Figure 1):
TLA = 2Ln√
D21 + D
22 .
(1)
Equation 1 describes the needle shape as a rhomboid. The
variables D1 and D2 are given in anatomical terms, i.e., upper
and lower surface, and accordingly, thickness and width of a
leaf are determined by the disposition of leaf xylem and
phloem. In P. abies, needle thickness (1.15--1.5 mm) is usually
larger and less variable than needle width (0.4--1.5 mm)
(Aussenac 1973, Frey 1981), and the needles are oriented in
space so that the mean angle between the largest projections
and the horizon is less for D1 than for D2. Therefore, needle
thickness and width, defined in this way, are homologous to
leaf width and thickness of broad-leaved species, respectively.
One measure of projected needle surface area (PLA) was
calculated as:
PLA 1 = Ln (Ld + z ),
(2)
where Ld is needle side length, and Ld + z is equal to projected
D1 (Figure 1). Assuming D1 > D2, and substituting
z=
Ld =
D21 − D22
2√
D 21 + D
22
√
D21 + D
22
2
and
gives
Figure 1. Geometrical model of a needle: D1 = needle thickness, D2 =
needle anatomical width, Ld = side length, NH = needle height, and
Ld + z = projected needle thickness.
IRRADIANCE AND TREE SIZE ON NEEDLE MORPHOLOGY
D21
PLA1 = Ln 2
.
2
D1 + D
2
√
(3)
Another measure for PLA was calculated as:
PLA 2 = Ln D1.
needles at 85 °C for 48 h, and needle dry weight per TLA and
PLA1 (LWAt and LWAp, respectively), and needle density (ND)
were calculated. Because LWAt is the product of leaf density
and thickness (Witkowski and Lamont 1991), or for P. abies,
of ND and needle height (NH, projection of needle width,
Figure 1), it can be computed as:
(4)
The value of PLA2 is always larger than the value of PLA1. The
geometric estimate, PLA1, was considered to be closer to the
PLA in the natural needle position on a shoot and was therefore
used in our study (except as noted). Nevertheless, no qualitative differences in relationships occurred when Equation 4 was
used instead of Equation 3. Steele et al. (1989) found that
measurements made with a photoelectric planimeter significantly underestimated PLA in Picea sitchensis (Bong.) Carr.
when compared to a geometric model. Accordingly, we expected PLA, measured directly by a video device or photoelectric planimeter, for needles spread on a flat surface to be in
between the geometric estimates PLA2 and PLA1, because
needles are often curved or twisted in shape. Furthermore, as
D2 or D1 change, probabilities for arranging the needles on D1
or on projected D1 and consequently, measuring PLA in the
direction of Ld + z or D1 also change. To test this assumption,
calculations based on Equations 3 and 4 were compared to
estimates of PLA measured with a video areameter (DIAS,
Delta-T Devices, Cambridge, U.K.) that was previously calibrated as described by Diebolt and Mudge (1988). On average,
Equation 3 underestimated projected needle area (PLAm) by
9.5%, and Equation 4 overestimated PLAm by 13% (Figure 2),
indicating that PLA measurements were sensitive to the variability in needle morphology.
Needle volume (V) was calculated as:
D1 D2
V = Ln
.
2
309
(5)
Needle weight (Mn) was determined after oven-drying the
LWAt =
Mn
V
= ND
,
TLA
TLA
where
(6)
D 1 D2
V
NH
=
=
.
TLA 4√
4
D21 + D
22
(7)
Often, shoot structure is characterized by the ratio of shoot
silhouette area to total needle surface area (STAR), where
shoot silhouette area is defined as the total shadow cast by a
shoot when the radiation beam is perpendicular to the shoot
axis (e.g., Boyce 1993). Assuming that all needles lie in the
same plane, side by side, then the possible maximum value,
STARcal, can be calculated when needle number per shoot (N),
shoot length (Ls), needle thickness (D1), PLA and TLA are
known:
STARcal =
PLA 2
,
TLA × SF
(8)
where SF is a factor accounting for possible space limitations
due to the variation in needle number per shoot length. If
D1N/(2Ls) > 1, there are more needles per shoot than can be
accommodated according to the definition of STARcal, resulting in needle overlap and shading between needles, and SF =
D1N/(2Ls). However, if D1N/(2Ls) ≤ 1, all needles can theoretically be placed in the same plane, side by side, and SF = 1. The
variable PLA2 is used because the maximum value of STARcal
is of interest.
Linear correlation and regression techniques were used to
analyze the data. Statistical relationships were considered significant if P < 0.05. All abbreviations and respective units are
listed in Appendix 1.
Results
Total tree height and ad were not correlated (P > 0.2). Relative
sampling height (Rh) was significantly correlated with light
availability (P < 0.001), and ad decreased nonlinearly with
decreasing Rh. Total tree height and Rh were not significantly
related. Thus, the effects of total tree height and ad on needle
structure could be studied independently.
Figure 2. Comparison between projected needle surface area measured
by a video areameter, PLAm (mm2), and PLAc (mm2) calculated from
measured needle parameters using Equations 3 (PLA1, d) and 4
(PLA2, s): PLAm = 1.02PLA1 + 1.00 (r2 = 0.934, P < 0.001, n = 36),
and PLAm = 0.89PLA2 − 0.38 (r2 = 0.958, P < 0.001, n = 36). For both
regression equations, the intercept did not differ significantly from
zero.
Needle dimensions and surface area
Needle thickness was not significantly related to irradiance
(Figure 3A). In contrast, needle width increased significantly
with ad (P < 0.00001, Figure 3B). As a result, D1/D2 decreased
(Figure 3C) and TLA/PLA increased (Figure 3D) linearly as
irradiance increased (P < 0.00001).
310
NIINEMETS AND KULL
Figure 3. Effects of relative irradiance (ad) on needle dimensions
and surface area. (A) Needle
thickness (D1, mm) versus ad: D1
= 0.17ad + 1.06 (r2 = 0.085, P >
0.2, n = 18). (B) Needle anatomical width (D2, mm) versus ad: D2
= 0.68ad + 0.46 (r2 = 0.730, P <
0.00001, n = 18). (C) D1/D2 versus ad: D1/D2 = −1.11ad + 2.05 (r2
= 0.829, P < 0.00001, n = 18).
(D) Total leaf area to projected
leaf area ratio (TLA/PLA) versus
ad: TLA/PLA = 2.40 + 1.06ad (r2
= 0.719, P < 0.00001, n = 18).
There was a tendency for PLA1/PLAm (Figure 2) to decrease
with D1/D2 (PLA1/PLAm = 1.34 − 0.19D1/D2, r2 = 0.315, P <
0.001, n = 36), and PLA2/PLAm to increase with D1/D2
(PLA2/PLAm = 0.76 + 0.08D1/D2, r2 = 0.127, P < 0.05, n = 36).
Consequently, with respect to measured PLA, underestimation
of PLA1 increased with decreasing D1/D2 (higher ad), and
overestimation of PLA2 increased at higher D1/D2 values
(lower ad) compared with measurements made with a video
areameter.
Total and projected needle surface areas (TLA and PLA) and
needle length were not significantly related to irradiance. No
correlations were found between total tree height and measured needle dimensions. There was a tendency for needle
length to increase with total tree height, but this was not
significant at P < 0.05.
The ratio of computed shoot silhouette area to total needle
surface area (STARcal) decreased significantly with increasing
ad (Figure 4). Tree height did not influence STARcal.The quantity D1N/(2Ls) (Equation 8) increased with increasing light and
tree height (r2 = 0.748, P < 0.0001).
Needle weight per area, volume, density and height
Needle volume and surface area of needle transverse sections
(0.5D1 × D2) were significantly correlated with ad (r2 = 0.272
and 0.315, respectively, P < 0.05). Needle dry weight per total
surface area (LWAt) and per projected surface area (LWAp)
increased with increasing ad and tree height (P < 0.00001,
Figures 5A and 5B). The value of LWAp, equal to
TLA
LWAp = LWAt
,
PLA
(9)
was more strongly related to ad than LWAt as a result of the
relationship between TLA/PLA and ad.
Variation in LWA with increasing total tree height and ad was
examined in more detail by considering the components of
LWA, needle density and needle height (Equations 6 and 7).
Needle density increased with total tree height (P < 0.00001,
Figure 6A) but was not correlated with ad (Figure 6B). The
ratio of needle volume to TLA (Equation 7) was linearly
related to ad (P < 0.00001, Figure 6D), but it was independent
of total tree height (Figure 6C). Both LWAt and LWAp were
correlated positively with NH and ND. Thus, the dependence
of LWA on ad can be attributed to changes in needle height,
whereas increases in LWA with total tree height can be attributed to increasing needle density. The correlation between
needle height and density was not significant (r2 = 0.009, P >
0.95).
Discussion
Needle dimensions and surface area
Figure 4. Calculated (Equation 8) shoot silhouette area to total needle
surface area ratio (STARcal) versus ad. The value of STARcal combines
the changes in projected to total leaf area ratio and needle number per
unit shoot length. STARcal = −0.174ad + 0.456 (r2 = 0.529, P < 0.001,
n = 17).
Because of the complex nature of needle geometry in P. abies
(e.g., Kerner et al. 1977), needle morphology was only approximated by a rhomboid. Frey (1981) evaluated many geometrical formulas for P. abies and found that the rhomboidal
model (Equation 1) gave the most reliable estimates of TLA
IRRADIANCE AND TREE SIZE ON NEEDLE MORPHOLOGY
311
Figure 5. Needle dry weight per
area in relation to total tree height
(m) and ad. (A) Needle weight per
TLA (LWAt, g m −2): LWAt =
0.635(tree height) + 29.7ad + 35.8
(r2 = 0.829, P < 0.00001, n = 17).
(B) Needle weight per PLA
(LWAp, g m − 2, Equation 9):
LWAp = 1.79(tree height) +
157ad + 75.0 (r2 = 0.874, P <
0.00001, n = 17).
Figure 6. Effects of total tree
height (m) and ad on needle density (ND, g cm −3) and needle volume per TLA (V/TLA, mm3
mm −2). (A) ND versus total tree
height: ND = 0.0035(tree height)
+ 0.33 (r2 = 0.761, P < 0.00001,
n = 17). (B) ND versus ad: ND =
0.021ad + 0.381 (r2 = 0.006, P >
0.8, n = 17). (C) V/TLA versus
tree height: V/TLA = 0.00066(tree
height) + 0.136 (r2 = 0.110, P >
0.2, n = 18). (D) V/TLA versus
ad: V/TLA = 0.107ad + 0.110 (r2
= 0.605, P < 0.001, n = 18).
over a wide range of D1/D2 ratios. However, compared to TLA
calculated as the product of needle perimeter and length,
Ivanov’s formula (Equation 1) underestimated TLA by a factor
of 0.94 in Picea rubens Sarg. (Boyce 1993) and 0.92--0.95 in
P. abies (Frey 1981), because the real needle perimeter was
longer than that predicted from the rhomboidal model. Nevertheless, precise estimation of TLA was not critical for the
qualitative relationships presented here, because the error due
to underestimated TLA was less than the variation due to total
tree height and ad. Moreover, because PLA, measured for
detached needles laid out on a flat surface varies systematically
with changing D1/D2, estimation of projected area based on a
geometrical model may be more explicit.
There is, at least up to a certain age, a strong relationship
between height and age of woody plants, thus tree height could
serve as an estimate of tree age. Although needle parameters,
except for needle weight per area and needle density, were not
dependent on total tree height, many needle morphological
traits correlate with tree age, e.g., SLA, D1, TLA and Mn in
P. sitchensis (Steele 1984, Steele et al. 1989) and Pinus radiata
D. Don (M. Steele, personal communication). Variation in
needle morphology with age in P. sitchensis was nonlinear,
whereas needle structure changed more rapidly in younger
plants (1 to 10 years old) than in older plants (over 10 years
old). Large spatial extensions and the long life spans of trees
make it difficult to study the effects of light availability and
tree age on foliage structure independently in the same stand,
but with grafted conifer scions placed in approximately the
same irradiance, variations in several needle parameters, e.g.,
Ln and Mn in Pinus taeda L. (Greenwood 1984), and Ln in Larix
laricina (Du Roi) K. Koch (Greenwood et al. 1989), were
related only to scion age. Thus, our a priori assumption that
variation in total tree height and associated changes in water
relations are the mechanistic reason for variation in needle
parameters with tree age may not be fully justified.
Leverenz and Jarvis (1980) reported that sun needles of
P. sitchensis had greater D1 and PLA than shade needles. No
relationships between ad and needle surface area (PLA and
TLA) or D1 were found in our study, whereas D2 was significantly correlated with ad. Because pronounced gradients of
light and needle development exist within a conifer shoot, the
morphological parameters vary considerably (Frey 1981, Frey
and Ivask 1983, Chandler and Dale 1990, Brewer et al. 1992,
Powell 1992), and 10 randomly taken needles per shoot may
not be sufficient to detect all structural differences caused by
the light environment. However, Brewer et al. (1992) reported
312
NIINEMETS AND KULL
that, in Abies fraseri (Pursh) Poir., D1 and D2 were relatively
constant at different positions within the shoot. Furthermore,
Powell (1992) found that in Tsuga canadensis (L.) Carr.,
several structural parameters of needles were related to shoot
length, which characterizes shoot vigor rather than light availability. Accordingly, one might conclude that several modifications in needle morphology may in fact be unrelated to
irradiance.
Koch (1976) reported that D2/D1 is dependent on irradiance,
and a quasi-linear relationship between D1/D2 and relative
irradiance, as was found in our study, has been found previously in P. abies (Aussenac 1973, Greis and Kellomäki
1981). Similarly, Jordan and Smith (1993) reported that needle
thickness was significantly lower in shade leaves than in sun
leaves of Abies lasiocarpa (Hook.) Nutt., and the ratio of
needle thickness to width was greater for sun needles, corresponding to our results (Figures 3B and 3C) (cf. Material and
methods). Recalculation of the data reported by Aussenac
(1973) for Abies nordmanniana (Steven) Spach. and Pseudotsuga menziesii (Mirb.) Franco resulted in a similar relationship. A constant value for TLA/PLA has been used to calculate
TLA or PLA in conifers when only one of them is measured.
Values reported include 2.429 for Abies balsamea (L.) Mill.
(Boyce 1993), 2.26 for Abies concolor (Gord.) Lindl. ex
Hildebr., 2.41 for Abies magnifica A. Murr. (Westman 1987),
2.57 for Pinus sylvestris L. (Roberts et al. 1982), 2.714 for
P. rubens (Boyce 1993), and 2.5 (Oren et al. 1986), 2.6 (Zimmermann 1990), 2.61 (Münster-Swendsen 1987) and 2.74
(Riederer et al. 1988) for P. abies. However, because of the
relationship between D1/D2 and irradiance, the ratio of total to
projected needle area also changes with light conditions in the
canopy. Consequently, TLA may be substantially underestimated in the upper canopy and overestimated in the lower
canopy when calculated based on a constant ratio of
TLA/PLA. Furthermore, changing patterns of TLA/PLA with
irradiance implies that the shoot silhouette area to total needle
area ratio (STAR), a parameter often used exclusively to characterize shoot structure, is likely to vary with needle morphology and ad (Figure 4). However, changes in STAR, resulting
from changing PLA/TLA of needles, can be influenced by
variation in the distribution of needles on a shoot (Niinemets
and Kull, unpublished results), e.g., increases in D1N/(2Ls)
with increasing ad results in decreasing STARcal with increasing ad even if TLA/PLA is constant.
There are methodological problems associated with the use
of different quantities in calculating physiological parameters
(Verduin 1959, Charles-Edwards and Ludwig 1975, Öquist et
al. 1982, ermák 1989, Smith et al. 1991, Jordan and Smith
1993). For example, photosynthetic capacity per needle dry
weight is equal to (photosynthetic capacity per needle
area)/LWA. The value of LWAp contains variations both in
TLA/PLA and LWAt (Equation 9). Additionally, the rates of
physiological processes based on different denominators, e.g.,
PLA, TLA, V and Mn, are not readily comparable when respective irradiances are not known. Moreover, when different species are compared, interspecific differences in needle morphology versus light relationships may need to be considered.
Needle weight per area, volume, density and height
The independent components of LWAt, needle height and
needle density, showed qualitatively different behavior with
respect to total tree height and irradiance. An increase in needle
height (projected needle width, D2) with ad is comparable to an
increase in leaf thickness with light in broad-leaved species,
thus characterizing the effect of light on cell size and division
(Jackson 1967, Nobel 1977, Nobel and Hartsock 1981,
Malkina 1983, Nygren and Kellomäki 1983). Because of the
dependence of needle height on light, other parameters, e.g., V
and the area of a needle transverse section (Figures 3B and
6D), were also correlated with ad. Similarly, in Picea schrenkiana Fisch. et C.A. Mey., needles from the southern aspect
(higher irradiance) had more and larger mesophyll cells, resulting in a significantly higher needle transverse section area
(Baidavletova 1984), than those from the northern aspect
(lower irradiance). Frey (1981) reported that sun needles of
P. abies have six to eight layers of mesophyll cells and shade
needles two to three layers in the direction of needle width
(D2), whereas for D1, the number of cell layers was similar
(seven to nine). Thus, the increase in needle height and V/TLA
with increasing irradiance could be attributed to a change in
needle width (D2). In an ecological context, enhanced leaf
thickness may be advantageous, resulting in an increase in leaf
mesophyll area per surface area and consequently, increasing
the diffusive conductance of the mesophyll to CO2 (Nobel
1977). Moreover, greater light absorptance, due to increasing
path length, is expected in thick leaves compared to thin leaves
(Öquist et al. 1982).
Variation in leaf density can be attributed to differences in
chemical composition and anatomical structure of leaves (accumulation of metabolites such as starch, differences in composition and thickness of cuticle and cell walls, cell size, and
frequency and size of intercellular spaces) (Rascio et al. 1990,
Witkowski and Lamont 1991). The significance of increasing
needle density with total tree height is not easily explained.
Accumulation of certain metabolites could indicate decreased
sink capacities for photosynthate utilization as growth rates
decrease with increasing tree age. On the other hand, as environmental stresses increase with total tree height, it may be
necessary to build needles that are increasingly resistant, i.e.,
have less intercellular spaces, a thicker cuticle and thick cell
walls. Indeed, indirect data show that the actual amount of
photosynthesizing tissue per unit leaf weight decreases with
increasing tree age or height. Older P. abies trees grown in
open areas have lower TLA- and weight-based photosynthetic
capacities than younger trees (Kull and Koppel 1987). It appears that needles, with the same area for light interception and
gaseous exchange, have higher carbon cost in taller and older
trees because needle density and LWA increase. Kull and
Niinemets (1993) proposed that the carbon requirement for
supporting tissues is larger in crowns of tall trees than in
crowns of small trees because of the need to survive water
deficits and lower water potentials. Although the change in
water potential due to gravitational force is only about 0.01
MPa m −1, gradients of water potential between 0.1 and 0.2
MPa m −1 have been reported in stems of P. sitchensis
IRRADIANCE AND TREE SIZE ON NEEDLE MORPHOLOGY
(Hellkvist et al. 1974). These gradients may be sufficiently
large to cause differences in needle morphology.
Acknowledgments
Dr. Ron J. Ryel (Dept. Range Science, Utah State University, USA)
and Prof. Dr. John D. Tenhunen (LS Pflanzenökologie, BITÖK, Universität Bayreuth, Germany) are gratefully acknowledged for their
invaluable comments on earlier drafts of this manuscript.
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IRRADIANCE AND TREE SIZE ON NEEDLE MORPHOLOGY
Appendix 1. Abbreviations and units.
Abbreviation
Definition
Unit
ad
D1
D2
Ld
Ld + z
Ln
Ls
LWAt
LWAp
Mn
SF
N
ND
NH
PLA
PLAc
PLA1
PLA2
PLAm
Rh
TLA
V
STARcal
Diffuse site factor
Needle thickness
mm
Needle width
mm
Needle side length
mm
Projected D1
mm
Needle length
mm
Shoot length
mm
Mn per TLA
g m −2
Mn per PLA1
g m −2
Needle dry weight
µg
Factor of needle spacing
Needle number per shoot
Needle density
g cm −3
Needle height (projected D2)
mm
Projected needle surface area
mm2
Calculated PLA (PLA1, PLA2)
mm2
PLAc (Equation 3)
mm2
PLAc (Equation 4)
mm2
Measured PLA
mm2
Relative sampling height
Total needle surface area
mm2
Needle volume
mm3
Calculated shoot silhouette area to TLA ratio
315