Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol15.1995:
Tree Physiology 15, 361--370
© 1995 Heron Publishing----Victoria, Canada
Gas exchange, leaf structure and nitrogen in contrasting successional
tree species growing in open and understory sites during a drought
MARC D. ABRAMS and SCOTT A. MOSTOLLER
School of Forest Resources, The Pennsylvania State University, 4 Ferguson Building, University Park, PA 16802, USA
Received April 14, 1994
Summary Seasonal ecophysiology, leaf structure and nitrogen were measured in saplings of early (Populus grandidentata
Michx. and Prunus serotina J.F. Ehrh.), middle (Fraxinus
americana L. and Carya tomentosa Nutt.) and late (Acer
rubrum L. and Cornus florida L.) successional tree species
during severe drought on adjacent open and understory sites in
central Pennsylvania, USA. Area-based net photosynthesis (A)
and leaf conductance to water vapor diffusion (gwv) varied by
site and species and were highest in open growing plants and
early successional species at both the open and understory sites.
In response to the period of maximum drought, both sunfleck
and sun leaves of the early successional species exhibited
smaller decreases in A than leaves of the other species. Shaded
understory leaves of all species were more susceptible to
drought than sun leaves and had negative midday A values
during the middle and later growing season. Shaded understory
leaves also displayed a reduced photosynthetic light response
during the peak drought period. Sun leaves were thicker and
had a greater mass per area (LMA) and nitrogen (N) content
than shaded leaves, and early and middle successional species
had higher N contents and concentrations than late successional species. In both sunfleck and sun leaves, seasonal A was
positively related to predawn leaf Ψ, gwv, LMA and N, and was
negatively related to vapor pressure deficit, midday leaf Ψ and
internal CO2. Although a significant amount of plasticity occurred in all species for most gas exchange and leaf structural
parameters, middle successional species exhibited the largest
degree of phenotypic plasticity between open and understory
plants.
Keywords: net photosynthesis, phenotypic plasticity, shading,
sunflecks, understory, water potential.
Introduction
Plants display nongenetic variation in morphology and physiology in response to environmental variation; a phenomenon
knwon as phenotypic plasticity (Bradshaw 1965, Schlichting
1986, Abrams 1994). Although many ecophysiological studies
have focused on phenotypic response to a single environmental
factor, such as temperature, light or water (Fryer and Ledig
1972, Bazzaz and Carlson 1982, Abrams and Kubiske 1990,
Walters et al. 1993, Kloeppel et al. 1993), there have been few
studies of phenotypic variation in relation to multiple stress
interactions (Osmond 1983, Vance and Zaerr 1991).
Tree species of varying successional status exhibit differences in ecophysiological responses and leaf structural characteristics. For example, early successional species often have
higher light-saturated gas exchange rates, less non-stomatal
inhibition of photosynthesis, lower osmotic potentials and
more xerophytic leaves than late successional species (Bazzaz
and Carlson 1982, Abrams and Kubiske 1990, Abrams et al.
1994, Kubiske and Abrams 1993, 1994). High gas exchange
rates in many species are associated with high leaf nitrogen
concentrations, although few studies have compared N concentrations in early versus late successional tree species or in
high- versus low-light phenotypes in relation to gas exchange
rates (Reich et al. 1990, Ellsworth and Reich 1992). Early
successional species may be capable of a wider range of
phenotypic responses than middle or late successional species
(Bazzaz 1979); however, there is little empirical evidence of
this phenomenon in tree species (Bazzaz and Carlson 1982,
Teskey and Shrestha 1985).
We measured seasonal gas exchange, water potential, leaf
structure, leaf nitrogen and the microenvironment during a
seasonal drought in six early, middle and late successional
broadleaf tree species in adjacent open and understory sites in
central Pennsylvania, USA. We used the data to test four
hypotheses: (1) understory plants are more susceptible to
drought from multiple stress interactions than open-growing
plants, (2) early successional plants have higher gas exchange
rates during well-watered and drought conditions in both open
and understory sites than middle and late successional species,
(3) physiological and morphological plasticity to open and
understory environments vary among early, middle and late
successional species, and (4) seasonal variations in ecophysiology among the contrasting species is related to variations in
microenvironment, leaf structure and nitrogen in the open and
understory environments.
Materials and methods
Study site
The study site is located approximately 4 km north of State
College, in central Pennsylvania (40°48′52″ N, 77°55′50″ W).
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ABRAMS AND MOSTOLLER
Average monthly minimum winter temperatures (December-February) range from −5 to − 7 °C, and average maximum
summer temperatures (June--August) range from 26 to 28 °C.
Average monthly precipitation varies from 6.5 to 10.3 cm, with
a total average annual precipitation of 97.9 cm. Braker (1981)
characterized the soil as a deep, well-drained cherty limestone
derivative with moderate permeability and high available
water capacity. Soil texture is silt loam on the surface horizon
and clay loam at 50 cm.
The study site included a 100-year-old relatively undisturbed valley floor forest dominated by oak (Quercus alba L.
and Q. velutina Lamb.) in the overstory and by mixed mesophytic species, including Acer rubrum L., Prunus serotina J.F.
Ehrh. and Fraxinus americana L., in the understory. A portion
of this forest was clear-cut in 1986, and presently supports a
diverse mixture of sapling-sized tree species. We selected
saplings (between 1.4 and 3.0 m in height) from six species of
contrasting successional status that occurred in both the mature
forest understory and the adjacent clear-cut: A. rubrum and
Cornus florida L. for the late successional group, F. americana
and Carya tomentosa Nutt. for the middle successional group,
and Populus grandidentata Michx. and P. serotina for the early
successional group (cf. Burns and Honkala 1990). We studied
five saplings per species.
Data collection
During the 1993 growing season, midday (1100--1300 h solar
time) microenvironmental and plant ecophysiological measurements were made at the open and understory sites at 6--15day intervals (n = 9) between May 27 and August 31 on
relatively cloud-free days. All ecophysiological measurements
were conducted on first flush or early season leaves. Predawn
(0600 h solar time) leaf water potential (Ψ ) was measured on
each sampling date on one leaf from each sapling with a
pressure chamber (PMS Instrument Co., Corvallis, OR). Midday gas exchange, photosynthetic photon flux density (PPFD),
and Ψ were measured on one mid-canopy leaf from each
sapling. For the compound-leaf species, F. americana and
C. tomentosa, gas exchange measurements were made on the
terminal leaflet. Gas exchange, leaf temperature and PPFD
measurements were made with an open-flow infrared gas
analysis system (LCA-3, Analytical Development Co., Herts,
U.K.). On the open site, only leaves that were in full sunlight
were measured. In the understory, two types of leaves were
measured, leaves growing in shade and leaves exposed to
occasional sunflecks. Leaves were allowed to acclimate to
sunflecks for a minimum of 15 min before measurement. Net
photosynthesis (A), leaf conductance to water vapor diffusion
(gwv), transpiration (J), leaf temperature, and vapor pressure
deficit (VPD) were calculated according to von Caemmerer
and Farquhar (1981). Gravimetric soil water of the upper 25
cm of soil was measured on four replicate samples from each
site at each date.
On June 23, 1993, midcanopy leaves from each sapling in
each species × site combination were collected for structural
and nitrogen (N) analyses. Leaf thickness was measured in
three places on each leaf at the approximate midpoint between
major veins by means of an ocular micrometer and light
microscope. Three measurements of guard cell length were
made and stomatal density was measured by means of acetate
impressions of the abaxial surface of each leaf (Payne 1968).
Leaf mass per area was calculated by dividing total area,
measured with an LI3100 leaf area meter (Li-Cor Inc., Lincoln,
NE), by dry weight (48 h at 80 °C). For the compound-leaf
species, leaf area and mass per area were measured using the
entire leaf, whereas leaf thickness, guard cell length and stomatal density were measured on the terminal leaflet. Leaf N
was analyzed by the Agricultural Analytical Services Laboratory at Penn State University using a micro-Kjeldahl digest and
an auto-analyzer. Additional measurements of leaf N and mass
per area were made on each sapling on August 5, 1993, to
evaluate temporal variation in these parameters (cf. Kloeppel
et al. 1993).
Statistical analyses for microenvironmental, leaf ecophysiological, structural and chemical parameters included oneway, two-way and repeated measures analysis of variance
(ANOVA) with general linear models, with time as a repeated
measures factor and site as the whole plot factor (SAS Institute
Inc., Cary, NC). Three-way ANOVA models with fixed effects
were used to partition the variation of A, gwv and Ψ among
sampling date, site, and species. Tukey’s multiple-range test
(P < 0.05) was used for all multiple comparisons. The interrelations between parameters were evaluated with Pearson product-moment correlation and least squares linear and nonlinear
regression analyses.
Results
Microenvironment
Daily average maximum and minimum monthly temperatures
from May through August 1993 were within 0.3--l.0 °C of the
30-year means (Figure 1). However, mean monthly precipitation was 52 and 41% below the 30-year mean for May and
June, respectively, and 16 and 18% below average for July and
August, respectively. Soil water decreased (P < 0.05) at both
the open and the understory study sites from a high of about
20% in late May and early June to about 10% in July and
August, but was generally not significantly different between
sites.
Seasonal mean photosynthetic photon flux density (PPFD)
differed significantly between sites, being highest in the open
site (1328 ± 23 µmol m −2 s −1) and lowest in the shaded
understory site (47 ± 3 µmol m −2 s −1) (Figure 2). Leaves in
understory sunflecks generally experienced decreasing PPFD
as the season progressed, ranging from 1000 to 350 µmol m −2
s −1 and averaging 743 ± 33 µmol m −2 s −1 for the season. Leaf
temperature increased during the season in all three light
regimes, and was generally highest (P < 0.05) in leaves at the
open site and lowest in understory leaves. Vapor pressure
deficit (VPD) varied with sampling dates, but was highest in
the open during the peak drought period and lowest in the
understory across all dates.
SUCCESSIONAL TREE SPECIES IN HIGH AND LOW IRRADIANCE
363
Figure 1. Mean (± SE) predawn leaf water
potential (Ψ) and soil water content at 0-25 cm depth at adjacent open and understory sites for nine sampling dates
(indicated by arrows) and maximum and
minimum air temperatures and daily precipitation during May, June, July and August 1993 for State College, Pennsylvania.
Gas exchange and leaf water potential
In general, for each species, midday net photosynthesis (A)
was high, intermediate and low in sun, sunfleck and shaded
leaves, respectively (Figure 3), except for P. grandidentata and
A. rubrum, where A in sun and sunfleck leaves was generally
not significantly different until later in the season when
drought effects were pronounced. Although A was low in all
understory leaves, it was positive for all species in late May
and June (overall mean = 0.05 to 0.45 µmol m −2 s −1), and
consistently near or below zero (P < 0.05) in July and August
(overall mean = −0.05 to −0.44 µmol m −2 s −1). Among species,
Prunus serotina had the highest seasonal understory A,
whereas P. grandidentata had the lowest understory A. For
sunfleck leaves, A was generally highest early in the season
and decreased (P < 0.05) during the season in most species,
with the exception of F. americana. In contrast, species at the
open site had more variable seasonal patterns of A, although,
in most species, it was lowest on July 24 at the peak of the
drought. From early to mid-season, A decreased across all
species by an average of 11, 36 and 193% in sun, sunfleck and
shaded leaves, respectively, (P < 0.05). Among the open-site
species, A. rubrum and C. florida had the largest relative
decreases in A (50 and 21%, respectively) from early to mid-
season.
Differences in gwv among species and light regimes were
less pronounced than those observed for A (Figure 4). Although most species had higher (P < 0.05) gwv in sun than in
understory leaves, gwv in sunfleck and understory leaves was
often not statistically different. Drought had little effect on gwv
on any sampling date, although gwv was slightly lower on July
24 than on other dates.
Predawn leaf water potential (Ψ) remained at − 0.2 MPa
from late May to early July, declined to −0.6 and −0.8 MPa in
the open and understory sites, respectively, by late July, then
increased during August at both sites (Figure 1). Predawn Ψ
was usually lower (P < 0.05) in shaded leaves than in sun
leaves, with seasonal means (± SE) of −0.41 ± 0.02 and −0.33
± 0.01 MPa, respectively, but it did not differ significantly
among species within each site.
For all species, midday Ψ was significantly lower in sun than
in shaded leaves (Figure 5). At both sites, there was a seasonal
decline (P < 0.05) in Ψ in all species except in A. rubrum. In
most species, there was a significant drop in midday Ψ during
the period of maximum drought (July 18--24).
For plants at the open site, seasonal mean A was highest
(P < 0.05) in the early successional species, P. grandidentata,
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ABRAMS AND MOSTOLLER
Figure 2. Mean (± SE) midday photosynthetic photon flux density
(PPFD), leaf temperature and vapor pressure deficit for sun (h),
sunfleck (r) and shaded (j) leaves for six successional tree species
at nine sampling dates.
P. serotina and middle successional species C. tomentosa, and
intermediate in F. americana (Figure 6). In shaded leaves,
seasonal A was not significantly different from zero for any
species. In sunfleck leaves, seasonal mean A was highest for
P. grandidentata, intermediate in P. serotina, and not significantly different among the other species. Mean gwv of sun
leaves followed the same ranking as A, except that the highest
value was observed in C. tomentosa. Mean gwv in shaded and
sunfleck leaves was highest in P. grandidentata and intermediate in P. serotina. Midday Ψ was lowest in P. grandidentata
and P. serotina at the open site and lowest in these species plus
F. americana in the understory. Measurements of Ψ were not
made on sunfleck leaves.
Partitioning of variances among sampling date, site, species
and the interaction terms indicated that 94% of the variance in
A was due to site. Although site was also the major source of
variation for gwv (57%) and Ψ (68%), sampling date (i.e.,
drought effects) and species differences combined explained
30--32% of the variation, and interactions among these factors
represented 1% of the variance.
There was a significant relationship between A and PPFD
for late May--June, but not for July (Figure 7). Only about 20%
of understory leaves had positive A values in July (mean A of
− 0.16 ± 0.06 µmol m −2 s −1) compared to 90% in late May-June (mean A of 0.23 ± 0.15 µ mol m −2 s −1), indicating that
drought decreased the photosynthetic light response in these
species.
Figure 3. Mean (± SE) midday net photosynthesis (A) at nine sampling dates for
sun (h), sunfleck (r) and shaded (j)
leaves of six tree species. Pogr = Populus
grandidentata, Prse = Prunus serotina,
Cato = Carya tomentosa, Fram = Fraxinus
americana, Acru = Acer rubrum, Cofl =
Cornus florida.
SUCCESSIONAL TREE SPECIES IN HIGH AND LOW IRRADIANCE
365
Figure 4. Mean (± SE) midday leaf conductance to water vapor diffusion (gwv) at
nine sampling dates for sun (h), sunfleck
(r) and shaded (j) leaves of six tree species: Pogr = Populus grandidentata, Prse
= Prunus serotina, Cato = Carya tomentosa, Fram = Fraxinus americana, Acru =
Acer rubrum, Cofl = Cornus florida.
Figure 5. Mean (± SE) midday leaf water
potential (Ψ) at nine sampling dates for
sun (h) and shaded (r) leaves of six tree
species: Pogr = Populus grandidentata,
Prse = Prunus serotina, Cato = Carya
tomentosa, Fram = Fraxinus americana,
Acru = Acer rubrum, Cofl = Cornus florida.
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ABRAMS AND MOSTOLLER
Figure 6. Seasonal mean (± SE) midday
net photosynthesis (A), leaf conductance
to water vapor diffusion (gwv) and midday
leaf water potential (Ψ) for sun, sunfleck
and shaded leaves of six tree species. Leaf
Ψ was not measured in sunfleck leaves.
Figure 7. Net photosynthesis (A) versus photosynthetic photon flux
density (PPFD) and fitted regression curve in shaded understory
leaves pooled for six tree species at six sampling dates (including the
predrought in June and peak drought in July). In July, A was not
significantly related to PPFD.
understory, whereas LMA was generally highest for F. americana at the open sites and highest for P. grandidentata in the
understory. In all species, leaf areas of sun leaves were similar
to those of shaded leaves. At both sites, leaf area was highest
in the compound-leaf species, F. americana and C. tomentosa,
and lowest in P. serotina. These three species also had longer
guard cells than the other species at both sites. In some species,
guard cells were larger and stomatal densities higher in sun
leaves than in shaded leaves.
Foliar nitrogen content (expressed as mass per area) was
higher in sun leaves than in shaded leaves of all species, even
though percent N was generally not significantly different
between sites (Table 2). Percent N varied among species, it was
lowest in the late successional species, A. rubrum and C. florida. Both sun and shaded leaves of these species also had low
N contents, as did shaded leaves of F. americana. Percent N
tended to decrease between June 23 and August 5, as LMA
increased in both shaded and sun leaves. Nitrogen content of
sun leaves tended to increase as the season progressed,
whereas N content of shaded leaves remained constant, except
for increases (P < 0.05) in C. tomentosa and P. grandidentata.
Leaf structure and nitrogen
Sun leaves were thicker (with the exception of P. serotina) and
had higher mass per area (LMA) than shaded leaves (Table 1).
Leaf thickness was highest in F. americana, C. tomentosa and
P. serotina at the open sites and highest in P. serotina in the
Interrelating gas exchange
Seasonal mean A in sun and sunfleck leaves was negatively
related to midday Ψ, VPD and internal CO2 (Ci), and was
positively related to early and late season leaf mass per area
SUCCESSIONAL TREE SPECIES IN HIGH AND LOW IRRADIANCE
367
Table 1. Leaf structural characteristics (mean ± SE) for six hardwood tree species in understory and open locations in central Pennsylvania. Leaves
collected on June 23 were measured for all five structural parameters, leaves collected on August 5 were only measured for leaf mass per area.
Location
Leaf
thickness
(µm)
Acer rubrum
Open
115.8 ± 4.9 c1
Under
88.8 ± 5.9 ab
Cornus florida
Open
124.2 ± 2.4 cd
Under
96.9 ± 1.5 b
Fraxinus americana
Open
151.5 ± 6.9 e
Under
85.8 ± 3.1 a
Carya tomentosa
Open
141.3 ± 15.4 de
Under
79.5 ± 2.4 a
Prunus serotina
Open
154.5 ± 8.2 e
Under
144.9 ± 5.0 e
Populus grandidentata
Open
118.8 ± 5.0 cd
Under
96.6 ± 1.0 b
1
Guard-cell
length
(µm)
Stomatal
density
(no. mm −2)
Leaf mass
per area 1
(mg cm − 2)
Leaf mass
per area 2
(mg cm − 2)
Leaf
area
(cm2)
13.35 ± 0.44 a
12.45 ± 0.38 a
371 ± 9 d
206 ± 16 c
5.24 ± 0.41de
3.55 ± 0.17bc
7.03 ± 0.48f
3.98 ± 0.21c
61.8 ± 7.2bc
72.4 ± 6.0 c
18.45 ± 0.91 bc
17.55 ± 0.77 b
56 ± 6 a
44 ± 3 a
4.10 ± 0.26 cd
2.66 ± 0.15 a
6.95 ± 0.72 ef
3.20 ± 0.19 b
58.5 ± 6.3 bc
49.0 ± 5.0 c
24.15 ± 0.96 ef
19.95 ± 0.18 c
79 ± 10 b
93 ± 16 b
6.49 ± 0.22 ef
2.86 ± 0.21 a
9.02 ± 0.34 g
3.92 ± 0.18 c
218.2 ± 44.7 d
266.9 ± 30.7 dc
26.55 ± 0.97 f
21.75 ± 0.53 d
240 ± 5 c
231 ± 6 c
5.32 ± 0.92 de
3.05 ± 0.06 ab
8.73 ± 1.14 fg
3.94 ± 0.09 c
312.5 ± 41.3 ef
296.1 ± 53.8 ef
23.70 ± 0.97 de
23.85 ± 0.37 e
232 ± 3 c
100 ± 3 b
5.24 ± 0.37 de
3.66 ± 0.11 bd
8.55 ± 0.55 fg
4.12 ± 0.08 c
22.3 ± 1.8 a
26.8 ± 3.8 a
12.30 ± 0.18 a
12.75 ± 0.41 a
354 ± 3 d
206 ± 3 c
5.77 ± 0.13 de
3.84 ± 0.08 bc
7.63 ± 0.35 fg
5.34 ± 0.26 d
45.0 ± 6.9 b
42.0 ± 6.2 b
Means within a column followed by the same letter are not significantly different at P < 0.05. When comparing leaf mass per area, means in
both columns followed by the same letter are not significantly different at P < 0.05.
Table 2. Mean (± SE) foliar nitrogen content (g m − 2) and % N for six hardwood tree species in understory versus open locations in central
Pennsylvania. Samples were collected on two dates during the 1993 growing season.
Location
Acer rubrum
Open
Under
Cornus florida
Open
Under
Fraxinus americana
Open
Under
Carya tomentosa
Open
Under
Prunus serotina
Open
Under
Populus grandidentata
Open
Under
1
June 23
August 5
g m −2
%N
g m −2
%N
0.98 ± 0.14 cd1
0.61 ± 0.05 e
1.89 ± 0.25 ab
1.70 ± 0.07 b
1.09 ± 0.03 c
0.60 ± 0.04 e
1.58 ± 0.11 ab
1.51 ± 0.05 a
0.79 ± 0.05 d
0.52 ± 0.02 e
1.92 ± 0.05 bc
1.97 ± 0.09 c
1.04 ± 0.11 cd
0.56 ± 0.04 e
1.50 ± 0.06 a
1.76 ± 0.10 b
1.31 ± 0.10 ab
0.57 ± 0.06 e
2.01 ± 0.13 bc
1.98 ± 0.09 c
1.59 ± 0.17 a
0.57 ± 0.08 e
1.76 ± 0.16 ab
1.71 ± 0.19 ab
1.17 ± 0.16 bc
0.70 ± 0.02 d
2.26 ± 0.14 cd
2.28 ± 0.04 d
1.93 ± 0.21 a
0.81 ± 0.01 b
2.25 ± 0.11 c
2.05 ± 0.05 bc
1.05 ± 0.08 cb
0.94 ± 0.07 b
2.05 ± 0.21 bc
2.57 ± 0.07 e
1.55 ± 0.12 a
0.87 ± 0.03 b
1.84 ± 0.19 b
2.10 ± 0.08 bc
1.42 ± 0.09 a
0.96 ± 0.12 b
2.46 ± 0.16 de
2.51 ± 0.12 e
1.70 ± 0.16 a
1.25 ± 0.02 c
2.24 ± 0.21 cd
2.37 ± 0.12 ce
Means of the same N parameter within a column or row followed by the same letter are not significantly different at P < 0.05.
(Figure 8). Seasonal A was positively correlated (r = 0.30) with
predawn Ψ. Both mean and maximum A per plant were positively related to early and late season N content.
Phenotypic plasticity
We compared phenotypic plasticity in light-saturated mean gas
exchange rates of sun and sunfleck leaves across the first three
sampling periods (May 27, June 11 and June 23) when PAR
values between sites were most similar (Figures 2 and 3). The
middle successional species, F. americana and C. tomentosa,
exhibited the largest relative differences in A and gwv between
sun and sunfleck leaves (81 to 114%) , whereas P. grandiden-
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ABRAMS AND MOSTOLLER
Figure 8. Interrelationships of net
photosynthesis (A) and selected
parameters for pooled data of
open leaves in six tree species.
Leaf mass per area and nitrogen
content (N) have separate regression lines for early (e) and late
(r) season.
tata exhibited the smallest differences (−14 to 4%). Fraxinus
americana and C. tomentosa also exhibited the highest degree
of phenotypic expression for leaf thickness (77--78%), guard
cell length (21--22%) and (LMA 122--130%), although C. florida and P. serotina also showed high plasticity for LMA (107-117%) (Table 1).
Discussion
Saplings in the open site experienced higher PPFD, leaf temperatures, and VPD than saplings in the understory. Saplings
in the open also had higher predawn Ψ than understory saplings, indicating less competition for soil water (cf. Abrams
1986, Kloeppel et al. 1993). This difference was most pronounced during the peak drought on July 24 when predawn Ψ
in open and understory study species varied by an average of
0.2 MPa. The increased opportunity for open-grown plants to
rehydrate overnight might be partially responsible for their
ability to maintain higher relative gas exchange rates than
understory plants during the drought (cf. Hinckley et al.
1978a).
During the drought period, gas exchange decreased more in
shaded leaves than in sun leaves of all species, resulting in A
values significantly less than zero in the shaded leaves. Decreased A coupled with decreased photosynthetic light response suggest that shaded leaves were more sensitive to
drought than sun leaves (cf. Abrams 1986, Abrams and Knapp
1986). Sunfleck leaves also exhibited a greater decrease in A
in response to the drought than sun leaves, indicating that
understory leaves have morphological and physiological limitations to high PPFD and drought compared with sun leaves.
However, A was positive in understory sunfleck leaves during
July and August, indicating that any potential carbon gain in
droughted understory plants at midday was derived from the
photosynthetic activity of sunfleck leaves. The large differences in seasonal A among shaded, sunfleck and sun leaves
accounted for almost all of the variance in A.
Despite large differences in A between sites, variation in gas
SUCCESSIONAL TREE SPECIES IN HIGH AND LOW IRRADIANCE
exchange in sun leaves was distinct along successional lines,
and there were smaller decreases in gas exchange in response
to the drought in early than in later successional species (cf.
Hinckley et al. 1978b, Bazzaz 1979, Bazzaz and Carlson 1982,
Bahari et al. 1985, Abrams and Knapp 1986, Abrams et al.
1994). Both mean and minimum midday Ψ values were lower
in the early successional species than in the later successional
species. There were also differences between shaded and sunfleck leaves in A, gwv and Ψ, indicating that the intrinsic
ecophysiological variation between early and late successional
species occurred, at least in the short-term, in both high and
low irradiance environments (cf. Bazzaz and Carlson 1982,
Abrams 1988, Kloeppel et al. 1993, Walters et al. 1993). In the
case of understory P. serotina, relatively high A values probably contributed to the success of this reputed early successional species in the understory of many forests in eastern
North America (Abrams 1992, Abrams et al. 1992, Horsley
and Gottschalk 1993).
Plants grown at high irradiances typically produce leaves
with greater thickness, mass per area, and stomatal density and
smaller area per leaf than plants grown at low irradiances
(Salisbury 1927, Jackson 1967, Carpenter and Smith 1981,
Abrams and Kubiske 1990). Similar differences are also apparent in early versus late successional and xeric versus mesic
species (Abrams and Kubiske 1990, Abrams et al. 1994). Leaf
thickness and mass per area were higher in open than in
understory plants and higher in early and middle successional
species than in late successional species, which may have
contributed to the increased drought tolerance in these plants
(cf. Abrams 1986, Abrams and Kubiske 1990, Abrams et al.
1994). The seasonal increase in leaf mass per area and its
positive relationship with A and gwv in sun and understory
sunfleck leaves are typical of many temperate hardwood species (Jurik 1986, Reich et al. 1991a, Kloeppel et al. 1993,
Abrams et al. 1994).
Leaf N content was highest in open growing, early and
middle successional species and increased during the growing
season. Similarly, Reich et al. (1990, 1991) reported higher
seasonal N content in early successional Rubus, Quercus and
Prunus species than in later successional Acer species. Higher
leaf N in early than in late successional species is consistent
with the physiological and morphological adaptations of early
successional species that result in high rates of photosynthesis
and growth in post-disturbance, high resource environments
(cf. Bazzaz 1979). Mean area-based A was positively related to
leaf N content or percent N, or both, in the open and understory
sunfleck leaves (cf. Field and Mooney 1986, Evans 1989,
Reich et al. 1990, 1991). Higher N content in sun leaves than
in shaded leaves is consistent with the idea that N acquisition
and allocation between plants and within canopies parallel
gradients of light availability (Björkman and Holmgren 1963,
Evans 1989, Ackerly 1992, Ellsworth and Reich 1992). However, percent N was generally not significantly different between shaded and sun leaves of the same species, indicating
that higher N content of sun leaves was predominantly a
function of increased LMA (cf. Björkman and Holmgren 1963,
Ackerly 1992). The finding that percent N did not vary be-
369
tween plants in the open and understory sites may reflect
differential N partitioning. In the understory, greater amounts
of N may be partitioned into chlorophyll, whereas in the open
more N may be partitioned into Rubisco, resulting in similar
percent N values between sites (Evans 1989).
It has been suggested that early successional plants may
have greater acclimation potential than later successional
plants (Bazzaz 1979, Bazzaz and Carlson 1982). However, our
results indicate that middle successional tree species may have
greater phenotypic plasticity than early or late successional
tree species. Middle successional species may have evolved
adaptations to a broader range of ecosystem conditions than
strictly early or late successional species, and therefore may be
capable of greater phenotypic plasticity (T.J. Givnish, personal
communication). Alternatively, successional status may not be
closely associated with phenotypic plasticity. For example, the
phenotypic plasticity exhibited by all our study species may be
a dominant mechanism by which trees respond to contrasting
microenvironmental conditions. Moreover, our study provides
an example of function following form, in which open growing
plants produced thicker leaves with higher mass per area and
N content than understory plants, which, in turn, permitted
higher gas exchange rates, lower leaf Ψ and greater tolerance
to drought. On the other hand, understory plants of all species
were able to maintain positive A at very low PAR early in the
season and A of sunfleck leaves often approached A of sun
leaves. Similar differences were apparent among the species,
with early and mid-successional species having higher leaf N,
A and mass per area and potentially greater tolerance to
drought than the late successional species.
Acknowledgments
We thank C.J. Mikan for providing field assistance and M.E. Kubiske
and D.A. Orwig for reviewing an earlier draft of the manuscript.
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© 1995 Heron Publishing----Victoria, Canada
Gas exchange, leaf structure and nitrogen in contrasting successional
tree species growing in open and understory sites during a drought
MARC D. ABRAMS and SCOTT A. MOSTOLLER
School of Forest Resources, The Pennsylvania State University, 4 Ferguson Building, University Park, PA 16802, USA
Received April 14, 1994
Summary Seasonal ecophysiology, leaf structure and nitrogen were measured in saplings of early (Populus grandidentata
Michx. and Prunus serotina J.F. Ehrh.), middle (Fraxinus
americana L. and Carya tomentosa Nutt.) and late (Acer
rubrum L. and Cornus florida L.) successional tree species
during severe drought on adjacent open and understory sites in
central Pennsylvania, USA. Area-based net photosynthesis (A)
and leaf conductance to water vapor diffusion (gwv) varied by
site and species and were highest in open growing plants and
early successional species at both the open and understory sites.
In response to the period of maximum drought, both sunfleck
and sun leaves of the early successional species exhibited
smaller decreases in A than leaves of the other species. Shaded
understory leaves of all species were more susceptible to
drought than sun leaves and had negative midday A values
during the middle and later growing season. Shaded understory
leaves also displayed a reduced photosynthetic light response
during the peak drought period. Sun leaves were thicker and
had a greater mass per area (LMA) and nitrogen (N) content
than shaded leaves, and early and middle successional species
had higher N contents and concentrations than late successional species. In both sunfleck and sun leaves, seasonal A was
positively related to predawn leaf Ψ, gwv, LMA and N, and was
negatively related to vapor pressure deficit, midday leaf Ψ and
internal CO2. Although a significant amount of plasticity occurred in all species for most gas exchange and leaf structural
parameters, middle successional species exhibited the largest
degree of phenotypic plasticity between open and understory
plants.
Keywords: net photosynthesis, phenotypic plasticity, shading,
sunflecks, understory, water potential.
Introduction
Plants display nongenetic variation in morphology and physiology in response to environmental variation; a phenomenon
knwon as phenotypic plasticity (Bradshaw 1965, Schlichting
1986, Abrams 1994). Although many ecophysiological studies
have focused on phenotypic response to a single environmental
factor, such as temperature, light or water (Fryer and Ledig
1972, Bazzaz and Carlson 1982, Abrams and Kubiske 1990,
Walters et al. 1993, Kloeppel et al. 1993), there have been few
studies of phenotypic variation in relation to multiple stress
interactions (Osmond 1983, Vance and Zaerr 1991).
Tree species of varying successional status exhibit differences in ecophysiological responses and leaf structural characteristics. For example, early successional species often have
higher light-saturated gas exchange rates, less non-stomatal
inhibition of photosynthesis, lower osmotic potentials and
more xerophytic leaves than late successional species (Bazzaz
and Carlson 1982, Abrams and Kubiske 1990, Abrams et al.
1994, Kubiske and Abrams 1993, 1994). High gas exchange
rates in many species are associated with high leaf nitrogen
concentrations, although few studies have compared N concentrations in early versus late successional tree species or in
high- versus low-light phenotypes in relation to gas exchange
rates (Reich et al. 1990, Ellsworth and Reich 1992). Early
successional species may be capable of a wider range of
phenotypic responses than middle or late successional species
(Bazzaz 1979); however, there is little empirical evidence of
this phenomenon in tree species (Bazzaz and Carlson 1982,
Teskey and Shrestha 1985).
We measured seasonal gas exchange, water potential, leaf
structure, leaf nitrogen and the microenvironment during a
seasonal drought in six early, middle and late successional
broadleaf tree species in adjacent open and understory sites in
central Pennsylvania, USA. We used the data to test four
hypotheses: (1) understory plants are more susceptible to
drought from multiple stress interactions than open-growing
plants, (2) early successional plants have higher gas exchange
rates during well-watered and drought conditions in both open
and understory sites than middle and late successional species,
(3) physiological and morphological plasticity to open and
understory environments vary among early, middle and late
successional species, and (4) seasonal variations in ecophysiology among the contrasting species is related to variations in
microenvironment, leaf structure and nitrogen in the open and
understory environments.
Materials and methods
Study site
The study site is located approximately 4 km north of State
College, in central Pennsylvania (40°48′52″ N, 77°55′50″ W).
362
ABRAMS AND MOSTOLLER
Average monthly minimum winter temperatures (December-February) range from −5 to − 7 °C, and average maximum
summer temperatures (June--August) range from 26 to 28 °C.
Average monthly precipitation varies from 6.5 to 10.3 cm, with
a total average annual precipitation of 97.9 cm. Braker (1981)
characterized the soil as a deep, well-drained cherty limestone
derivative with moderate permeability and high available
water capacity. Soil texture is silt loam on the surface horizon
and clay loam at 50 cm.
The study site included a 100-year-old relatively undisturbed valley floor forest dominated by oak (Quercus alba L.
and Q. velutina Lamb.) in the overstory and by mixed mesophytic species, including Acer rubrum L., Prunus serotina J.F.
Ehrh. and Fraxinus americana L., in the understory. A portion
of this forest was clear-cut in 1986, and presently supports a
diverse mixture of sapling-sized tree species. We selected
saplings (between 1.4 and 3.0 m in height) from six species of
contrasting successional status that occurred in both the mature
forest understory and the adjacent clear-cut: A. rubrum and
Cornus florida L. for the late successional group, F. americana
and Carya tomentosa Nutt. for the middle successional group,
and Populus grandidentata Michx. and P. serotina for the early
successional group (cf. Burns and Honkala 1990). We studied
five saplings per species.
Data collection
During the 1993 growing season, midday (1100--1300 h solar
time) microenvironmental and plant ecophysiological measurements were made at the open and understory sites at 6--15day intervals (n = 9) between May 27 and August 31 on
relatively cloud-free days. All ecophysiological measurements
were conducted on first flush or early season leaves. Predawn
(0600 h solar time) leaf water potential (Ψ ) was measured on
each sampling date on one leaf from each sapling with a
pressure chamber (PMS Instrument Co., Corvallis, OR). Midday gas exchange, photosynthetic photon flux density (PPFD),
and Ψ were measured on one mid-canopy leaf from each
sapling. For the compound-leaf species, F. americana and
C. tomentosa, gas exchange measurements were made on the
terminal leaflet. Gas exchange, leaf temperature and PPFD
measurements were made with an open-flow infrared gas
analysis system (LCA-3, Analytical Development Co., Herts,
U.K.). On the open site, only leaves that were in full sunlight
were measured. In the understory, two types of leaves were
measured, leaves growing in shade and leaves exposed to
occasional sunflecks. Leaves were allowed to acclimate to
sunflecks for a minimum of 15 min before measurement. Net
photosynthesis (A), leaf conductance to water vapor diffusion
(gwv), transpiration (J), leaf temperature, and vapor pressure
deficit (VPD) were calculated according to von Caemmerer
and Farquhar (1981). Gravimetric soil water of the upper 25
cm of soil was measured on four replicate samples from each
site at each date.
On June 23, 1993, midcanopy leaves from each sapling in
each species × site combination were collected for structural
and nitrogen (N) analyses. Leaf thickness was measured in
three places on each leaf at the approximate midpoint between
major veins by means of an ocular micrometer and light
microscope. Three measurements of guard cell length were
made and stomatal density was measured by means of acetate
impressions of the abaxial surface of each leaf (Payne 1968).
Leaf mass per area was calculated by dividing total area,
measured with an LI3100 leaf area meter (Li-Cor Inc., Lincoln,
NE), by dry weight (48 h at 80 °C). For the compound-leaf
species, leaf area and mass per area were measured using the
entire leaf, whereas leaf thickness, guard cell length and stomatal density were measured on the terminal leaflet. Leaf N
was analyzed by the Agricultural Analytical Services Laboratory at Penn State University using a micro-Kjeldahl digest and
an auto-analyzer. Additional measurements of leaf N and mass
per area were made on each sapling on August 5, 1993, to
evaluate temporal variation in these parameters (cf. Kloeppel
et al. 1993).
Statistical analyses for microenvironmental, leaf ecophysiological, structural and chemical parameters included oneway, two-way and repeated measures analysis of variance
(ANOVA) with general linear models, with time as a repeated
measures factor and site as the whole plot factor (SAS Institute
Inc., Cary, NC). Three-way ANOVA models with fixed effects
were used to partition the variation of A, gwv and Ψ among
sampling date, site, and species. Tukey’s multiple-range test
(P < 0.05) was used for all multiple comparisons. The interrelations between parameters were evaluated with Pearson product-moment correlation and least squares linear and nonlinear
regression analyses.
Results
Microenvironment
Daily average maximum and minimum monthly temperatures
from May through August 1993 were within 0.3--l.0 °C of the
30-year means (Figure 1). However, mean monthly precipitation was 52 and 41% below the 30-year mean for May and
June, respectively, and 16 and 18% below average for July and
August, respectively. Soil water decreased (P < 0.05) at both
the open and the understory study sites from a high of about
20% in late May and early June to about 10% in July and
August, but was generally not significantly different between
sites.
Seasonal mean photosynthetic photon flux density (PPFD)
differed significantly between sites, being highest in the open
site (1328 ± 23 µmol m −2 s −1) and lowest in the shaded
understory site (47 ± 3 µmol m −2 s −1) (Figure 2). Leaves in
understory sunflecks generally experienced decreasing PPFD
as the season progressed, ranging from 1000 to 350 µmol m −2
s −1 and averaging 743 ± 33 µmol m −2 s −1 for the season. Leaf
temperature increased during the season in all three light
regimes, and was generally highest (P < 0.05) in leaves at the
open site and lowest in understory leaves. Vapor pressure
deficit (VPD) varied with sampling dates, but was highest in
the open during the peak drought period and lowest in the
understory across all dates.
SUCCESSIONAL TREE SPECIES IN HIGH AND LOW IRRADIANCE
363
Figure 1. Mean (± SE) predawn leaf water
potential (Ψ) and soil water content at 0-25 cm depth at adjacent open and understory sites for nine sampling dates
(indicated by arrows) and maximum and
minimum air temperatures and daily precipitation during May, June, July and August 1993 for State College, Pennsylvania.
Gas exchange and leaf water potential
In general, for each species, midday net photosynthesis (A)
was high, intermediate and low in sun, sunfleck and shaded
leaves, respectively (Figure 3), except for P. grandidentata and
A. rubrum, where A in sun and sunfleck leaves was generally
not significantly different until later in the season when
drought effects were pronounced. Although A was low in all
understory leaves, it was positive for all species in late May
and June (overall mean = 0.05 to 0.45 µmol m −2 s −1), and
consistently near or below zero (P < 0.05) in July and August
(overall mean = −0.05 to −0.44 µmol m −2 s −1). Among species,
Prunus serotina had the highest seasonal understory A,
whereas P. grandidentata had the lowest understory A. For
sunfleck leaves, A was generally highest early in the season
and decreased (P < 0.05) during the season in most species,
with the exception of F. americana. In contrast, species at the
open site had more variable seasonal patterns of A, although,
in most species, it was lowest on July 24 at the peak of the
drought. From early to mid-season, A decreased across all
species by an average of 11, 36 and 193% in sun, sunfleck and
shaded leaves, respectively, (P < 0.05). Among the open-site
species, A. rubrum and C. florida had the largest relative
decreases in A (50 and 21%, respectively) from early to mid-
season.
Differences in gwv among species and light regimes were
less pronounced than those observed for A (Figure 4). Although most species had higher (P < 0.05) gwv in sun than in
understory leaves, gwv in sunfleck and understory leaves was
often not statistically different. Drought had little effect on gwv
on any sampling date, although gwv was slightly lower on July
24 than on other dates.
Predawn leaf water potential (Ψ) remained at − 0.2 MPa
from late May to early July, declined to −0.6 and −0.8 MPa in
the open and understory sites, respectively, by late July, then
increased during August at both sites (Figure 1). Predawn Ψ
was usually lower (P < 0.05) in shaded leaves than in sun
leaves, with seasonal means (± SE) of −0.41 ± 0.02 and −0.33
± 0.01 MPa, respectively, but it did not differ significantly
among species within each site.
For all species, midday Ψ was significantly lower in sun than
in shaded leaves (Figure 5). At both sites, there was a seasonal
decline (P < 0.05) in Ψ in all species except in A. rubrum. In
most species, there was a significant drop in midday Ψ during
the period of maximum drought (July 18--24).
For plants at the open site, seasonal mean A was highest
(P < 0.05) in the early successional species, P. grandidentata,
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ABRAMS AND MOSTOLLER
Figure 2. Mean (± SE) midday photosynthetic photon flux density
(PPFD), leaf temperature and vapor pressure deficit for sun (h),
sunfleck (r) and shaded (j) leaves for six successional tree species
at nine sampling dates.
P. serotina and middle successional species C. tomentosa, and
intermediate in F. americana (Figure 6). In shaded leaves,
seasonal A was not significantly different from zero for any
species. In sunfleck leaves, seasonal mean A was highest for
P. grandidentata, intermediate in P. serotina, and not significantly different among the other species. Mean gwv of sun
leaves followed the same ranking as A, except that the highest
value was observed in C. tomentosa. Mean gwv in shaded and
sunfleck leaves was highest in P. grandidentata and intermediate in P. serotina. Midday Ψ was lowest in P. grandidentata
and P. serotina at the open site and lowest in these species plus
F. americana in the understory. Measurements of Ψ were not
made on sunfleck leaves.
Partitioning of variances among sampling date, site, species
and the interaction terms indicated that 94% of the variance in
A was due to site. Although site was also the major source of
variation for gwv (57%) and Ψ (68%), sampling date (i.e.,
drought effects) and species differences combined explained
30--32% of the variation, and interactions among these factors
represented 1% of the variance.
There was a significant relationship between A and PPFD
for late May--June, but not for July (Figure 7). Only about 20%
of understory leaves had positive A values in July (mean A of
− 0.16 ± 0.06 µmol m −2 s −1) compared to 90% in late May-June (mean A of 0.23 ± 0.15 µ mol m −2 s −1), indicating that
drought decreased the photosynthetic light response in these
species.
Figure 3. Mean (± SE) midday net photosynthesis (A) at nine sampling dates for
sun (h), sunfleck (r) and shaded (j)
leaves of six tree species. Pogr = Populus
grandidentata, Prse = Prunus serotina,
Cato = Carya tomentosa, Fram = Fraxinus
americana, Acru = Acer rubrum, Cofl =
Cornus florida.
SUCCESSIONAL TREE SPECIES IN HIGH AND LOW IRRADIANCE
365
Figure 4. Mean (± SE) midday leaf conductance to water vapor diffusion (gwv) at
nine sampling dates for sun (h), sunfleck
(r) and shaded (j) leaves of six tree species: Pogr = Populus grandidentata, Prse
= Prunus serotina, Cato = Carya tomentosa, Fram = Fraxinus americana, Acru =
Acer rubrum, Cofl = Cornus florida.
Figure 5. Mean (± SE) midday leaf water
potential (Ψ) at nine sampling dates for
sun (h) and shaded (r) leaves of six tree
species: Pogr = Populus grandidentata,
Prse = Prunus serotina, Cato = Carya
tomentosa, Fram = Fraxinus americana,
Acru = Acer rubrum, Cofl = Cornus florida.
366
ABRAMS AND MOSTOLLER
Figure 6. Seasonal mean (± SE) midday
net photosynthesis (A), leaf conductance
to water vapor diffusion (gwv) and midday
leaf water potential (Ψ) for sun, sunfleck
and shaded leaves of six tree species. Leaf
Ψ was not measured in sunfleck leaves.
Figure 7. Net photosynthesis (A) versus photosynthetic photon flux
density (PPFD) and fitted regression curve in shaded understory
leaves pooled for six tree species at six sampling dates (including the
predrought in June and peak drought in July). In July, A was not
significantly related to PPFD.
understory, whereas LMA was generally highest for F. americana at the open sites and highest for P. grandidentata in the
understory. In all species, leaf areas of sun leaves were similar
to those of shaded leaves. At both sites, leaf area was highest
in the compound-leaf species, F. americana and C. tomentosa,
and lowest in P. serotina. These three species also had longer
guard cells than the other species at both sites. In some species,
guard cells were larger and stomatal densities higher in sun
leaves than in shaded leaves.
Foliar nitrogen content (expressed as mass per area) was
higher in sun leaves than in shaded leaves of all species, even
though percent N was generally not significantly different
between sites (Table 2). Percent N varied among species, it was
lowest in the late successional species, A. rubrum and C. florida. Both sun and shaded leaves of these species also had low
N contents, as did shaded leaves of F. americana. Percent N
tended to decrease between June 23 and August 5, as LMA
increased in both shaded and sun leaves. Nitrogen content of
sun leaves tended to increase as the season progressed,
whereas N content of shaded leaves remained constant, except
for increases (P < 0.05) in C. tomentosa and P. grandidentata.
Leaf structure and nitrogen
Sun leaves were thicker (with the exception of P. serotina) and
had higher mass per area (LMA) than shaded leaves (Table 1).
Leaf thickness was highest in F. americana, C. tomentosa and
P. serotina at the open sites and highest in P. serotina in the
Interrelating gas exchange
Seasonal mean A in sun and sunfleck leaves was negatively
related to midday Ψ, VPD and internal CO2 (Ci), and was
positively related to early and late season leaf mass per area
SUCCESSIONAL TREE SPECIES IN HIGH AND LOW IRRADIANCE
367
Table 1. Leaf structural characteristics (mean ± SE) for six hardwood tree species in understory and open locations in central Pennsylvania. Leaves
collected on June 23 were measured for all five structural parameters, leaves collected on August 5 were only measured for leaf mass per area.
Location
Leaf
thickness
(µm)
Acer rubrum
Open
115.8 ± 4.9 c1
Under
88.8 ± 5.9 ab
Cornus florida
Open
124.2 ± 2.4 cd
Under
96.9 ± 1.5 b
Fraxinus americana
Open
151.5 ± 6.9 e
Under
85.8 ± 3.1 a
Carya tomentosa
Open
141.3 ± 15.4 de
Under
79.5 ± 2.4 a
Prunus serotina
Open
154.5 ± 8.2 e
Under
144.9 ± 5.0 e
Populus grandidentata
Open
118.8 ± 5.0 cd
Under
96.6 ± 1.0 b
1
Guard-cell
length
(µm)
Stomatal
density
(no. mm −2)
Leaf mass
per area 1
(mg cm − 2)
Leaf mass
per area 2
(mg cm − 2)
Leaf
area
(cm2)
13.35 ± 0.44 a
12.45 ± 0.38 a
371 ± 9 d
206 ± 16 c
5.24 ± 0.41de
3.55 ± 0.17bc
7.03 ± 0.48f
3.98 ± 0.21c
61.8 ± 7.2bc
72.4 ± 6.0 c
18.45 ± 0.91 bc
17.55 ± 0.77 b
56 ± 6 a
44 ± 3 a
4.10 ± 0.26 cd
2.66 ± 0.15 a
6.95 ± 0.72 ef
3.20 ± 0.19 b
58.5 ± 6.3 bc
49.0 ± 5.0 c
24.15 ± 0.96 ef
19.95 ± 0.18 c
79 ± 10 b
93 ± 16 b
6.49 ± 0.22 ef
2.86 ± 0.21 a
9.02 ± 0.34 g
3.92 ± 0.18 c
218.2 ± 44.7 d
266.9 ± 30.7 dc
26.55 ± 0.97 f
21.75 ± 0.53 d
240 ± 5 c
231 ± 6 c
5.32 ± 0.92 de
3.05 ± 0.06 ab
8.73 ± 1.14 fg
3.94 ± 0.09 c
312.5 ± 41.3 ef
296.1 ± 53.8 ef
23.70 ± 0.97 de
23.85 ± 0.37 e
232 ± 3 c
100 ± 3 b
5.24 ± 0.37 de
3.66 ± 0.11 bd
8.55 ± 0.55 fg
4.12 ± 0.08 c
22.3 ± 1.8 a
26.8 ± 3.8 a
12.30 ± 0.18 a
12.75 ± 0.41 a
354 ± 3 d
206 ± 3 c
5.77 ± 0.13 de
3.84 ± 0.08 bc
7.63 ± 0.35 fg
5.34 ± 0.26 d
45.0 ± 6.9 b
42.0 ± 6.2 b
Means within a column followed by the same letter are not significantly different at P < 0.05. When comparing leaf mass per area, means in
both columns followed by the same letter are not significantly different at P < 0.05.
Table 2. Mean (± SE) foliar nitrogen content (g m − 2) and % N for six hardwood tree species in understory versus open locations in central
Pennsylvania. Samples were collected on two dates during the 1993 growing season.
Location
Acer rubrum
Open
Under
Cornus florida
Open
Under
Fraxinus americana
Open
Under
Carya tomentosa
Open
Under
Prunus serotina
Open
Under
Populus grandidentata
Open
Under
1
June 23
August 5
g m −2
%N
g m −2
%N
0.98 ± 0.14 cd1
0.61 ± 0.05 e
1.89 ± 0.25 ab
1.70 ± 0.07 b
1.09 ± 0.03 c
0.60 ± 0.04 e
1.58 ± 0.11 ab
1.51 ± 0.05 a
0.79 ± 0.05 d
0.52 ± 0.02 e
1.92 ± 0.05 bc
1.97 ± 0.09 c
1.04 ± 0.11 cd
0.56 ± 0.04 e
1.50 ± 0.06 a
1.76 ± 0.10 b
1.31 ± 0.10 ab
0.57 ± 0.06 e
2.01 ± 0.13 bc
1.98 ± 0.09 c
1.59 ± 0.17 a
0.57 ± 0.08 e
1.76 ± 0.16 ab
1.71 ± 0.19 ab
1.17 ± 0.16 bc
0.70 ± 0.02 d
2.26 ± 0.14 cd
2.28 ± 0.04 d
1.93 ± 0.21 a
0.81 ± 0.01 b
2.25 ± 0.11 c
2.05 ± 0.05 bc
1.05 ± 0.08 cb
0.94 ± 0.07 b
2.05 ± 0.21 bc
2.57 ± 0.07 e
1.55 ± 0.12 a
0.87 ± 0.03 b
1.84 ± 0.19 b
2.10 ± 0.08 bc
1.42 ± 0.09 a
0.96 ± 0.12 b
2.46 ± 0.16 de
2.51 ± 0.12 e
1.70 ± 0.16 a
1.25 ± 0.02 c
2.24 ± 0.21 cd
2.37 ± 0.12 ce
Means of the same N parameter within a column or row followed by the same letter are not significantly different at P < 0.05.
(Figure 8). Seasonal A was positively correlated (r = 0.30) with
predawn Ψ. Both mean and maximum A per plant were positively related to early and late season N content.
Phenotypic plasticity
We compared phenotypic plasticity in light-saturated mean gas
exchange rates of sun and sunfleck leaves across the first three
sampling periods (May 27, June 11 and June 23) when PAR
values between sites were most similar (Figures 2 and 3). The
middle successional species, F. americana and C. tomentosa,
exhibited the largest relative differences in A and gwv between
sun and sunfleck leaves (81 to 114%) , whereas P. grandiden-
368
ABRAMS AND MOSTOLLER
Figure 8. Interrelationships of net
photosynthesis (A) and selected
parameters for pooled data of
open leaves in six tree species.
Leaf mass per area and nitrogen
content (N) have separate regression lines for early (e) and late
(r) season.
tata exhibited the smallest differences (−14 to 4%). Fraxinus
americana and C. tomentosa also exhibited the highest degree
of phenotypic expression for leaf thickness (77--78%), guard
cell length (21--22%) and (LMA 122--130%), although C. florida and P. serotina also showed high plasticity for LMA (107-117%) (Table 1).
Discussion
Saplings in the open site experienced higher PPFD, leaf temperatures, and VPD than saplings in the understory. Saplings
in the open also had higher predawn Ψ than understory saplings, indicating less competition for soil water (cf. Abrams
1986, Kloeppel et al. 1993). This difference was most pronounced during the peak drought on July 24 when predawn Ψ
in open and understory study species varied by an average of
0.2 MPa. The increased opportunity for open-grown plants to
rehydrate overnight might be partially responsible for their
ability to maintain higher relative gas exchange rates than
understory plants during the drought (cf. Hinckley et al.
1978a).
During the drought period, gas exchange decreased more in
shaded leaves than in sun leaves of all species, resulting in A
values significantly less than zero in the shaded leaves. Decreased A coupled with decreased photosynthetic light response suggest that shaded leaves were more sensitive to
drought than sun leaves (cf. Abrams 1986, Abrams and Knapp
1986). Sunfleck leaves also exhibited a greater decrease in A
in response to the drought than sun leaves, indicating that
understory leaves have morphological and physiological limitations to high PPFD and drought compared with sun leaves.
However, A was positive in understory sunfleck leaves during
July and August, indicating that any potential carbon gain in
droughted understory plants at midday was derived from the
photosynthetic activity of sunfleck leaves. The large differences in seasonal A among shaded, sunfleck and sun leaves
accounted for almost all of the variance in A.
Despite large differences in A between sites, variation in gas
SUCCESSIONAL TREE SPECIES IN HIGH AND LOW IRRADIANCE
exchange in sun leaves was distinct along successional lines,
and there were smaller decreases in gas exchange in response
to the drought in early than in later successional species (cf.
Hinckley et al. 1978b, Bazzaz 1979, Bazzaz and Carlson 1982,
Bahari et al. 1985, Abrams and Knapp 1986, Abrams et al.
1994). Both mean and minimum midday Ψ values were lower
in the early successional species than in the later successional
species. There were also differences between shaded and sunfleck leaves in A, gwv and Ψ, indicating that the intrinsic
ecophysiological variation between early and late successional
species occurred, at least in the short-term, in both high and
low irradiance environments (cf. Bazzaz and Carlson 1982,
Abrams 1988, Kloeppel et al. 1993, Walters et al. 1993). In the
case of understory P. serotina, relatively high A values probably contributed to the success of this reputed early successional species in the understory of many forests in eastern
North America (Abrams 1992, Abrams et al. 1992, Horsley
and Gottschalk 1993).
Plants grown at high irradiances typically produce leaves
with greater thickness, mass per area, and stomatal density and
smaller area per leaf than plants grown at low irradiances
(Salisbury 1927, Jackson 1967, Carpenter and Smith 1981,
Abrams and Kubiske 1990). Similar differences are also apparent in early versus late successional and xeric versus mesic
species (Abrams and Kubiske 1990, Abrams et al. 1994). Leaf
thickness and mass per area were higher in open than in
understory plants and higher in early and middle successional
species than in late successional species, which may have
contributed to the increased drought tolerance in these plants
(cf. Abrams 1986, Abrams and Kubiske 1990, Abrams et al.
1994). The seasonal increase in leaf mass per area and its
positive relationship with A and gwv in sun and understory
sunfleck leaves are typical of many temperate hardwood species (Jurik 1986, Reich et al. 1991a, Kloeppel et al. 1993,
Abrams et al. 1994).
Leaf N content was highest in open growing, early and
middle successional species and increased during the growing
season. Similarly, Reich et al. (1990, 1991) reported higher
seasonal N content in early successional Rubus, Quercus and
Prunus species than in later successional Acer species. Higher
leaf N in early than in late successional species is consistent
with the physiological and morphological adaptations of early
successional species that result in high rates of photosynthesis
and growth in post-disturbance, high resource environments
(cf. Bazzaz 1979). Mean area-based A was positively related to
leaf N content or percent N, or both, in the open and understory
sunfleck leaves (cf. Field and Mooney 1986, Evans 1989,
Reich et al. 1990, 1991). Higher N content in sun leaves than
in shaded leaves is consistent with the idea that N acquisition
and allocation between plants and within canopies parallel
gradients of light availability (Björkman and Holmgren 1963,
Evans 1989, Ackerly 1992, Ellsworth and Reich 1992). However, percent N was generally not significantly different between shaded and sun leaves of the same species, indicating
that higher N content of sun leaves was predominantly a
function of increased LMA (cf. Björkman and Holmgren 1963,
Ackerly 1992). The finding that percent N did not vary be-
369
tween plants in the open and understory sites may reflect
differential N partitioning. In the understory, greater amounts
of N may be partitioned into chlorophyll, whereas in the open
more N may be partitioned into Rubisco, resulting in similar
percent N values between sites (Evans 1989).
It has been suggested that early successional plants may
have greater acclimation potential than later successional
plants (Bazzaz 1979, Bazzaz and Carlson 1982). However, our
results indicate that middle successional tree species may have
greater phenotypic plasticity than early or late successional
tree species. Middle successional species may have evolved
adaptations to a broader range of ecosystem conditions than
strictly early or late successional species, and therefore may be
capable of greater phenotypic plasticity (T.J. Givnish, personal
communication). Alternatively, successional status may not be
closely associated with phenotypic plasticity. For example, the
phenotypic plasticity exhibited by all our study species may be
a dominant mechanism by which trees respond to contrasting
microenvironmental conditions. Moreover, our study provides
an example of function following form, in which open growing
plants produced thicker leaves with higher mass per area and
N content than understory plants, which, in turn, permitted
higher gas exchange rates, lower leaf Ψ and greater tolerance
to drought. On the other hand, understory plants of all species
were able to maintain positive A at very low PAR early in the
season and A of sunfleck leaves often approached A of sun
leaves. Similar differences were apparent among the species,
with early and mid-successional species having higher leaf N,
A and mass per area and potentially greater tolerance to
drought than the late successional species.
Acknowledgments
We thank C.J. Mikan for providing field assistance and M.E. Kubiske
and D.A. Orwig for reviewing an earlier draft of the manuscript.
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