Annals of Botany 82 : 9–19, 1998
Diverse Responses of Maple Saplings to Forest Light Regimes
T H O M A S T. L E I* and M A R T I N J. L E C H O W I C Z
Department of Biology, McGill UniŠersity, 1205 AŠenue Docteur Penfield, Montreal, Quebec, Canada H3A 1B1
Received : 2 July 1997
Returned for revision : 28 January 1998
Accepted : 13 March 1998
Seedlings of 11 species of forest maples (Acer L.) were grown outdoors from budburst to senescence under three light
regimes : ‘ gap centre under clear skies ’ (approx. 20 % open sky irradiance ; red : far-red ratio ¯ 1±12) ; ‘ gap centre
under cloudy skies ’ (1±5 %, ratio ¯ 1±03) ; and ‘ gap edge ’ (2±5 %, ratio ¯ 0±6). Seedlings grown under the gap centre
(clear sky) regime had significantly greater height growth, greater specific leaf mass, higher root : shoot ratio, greater
investment in roots, higher leaf nitrogen concentrations, greater chlorophyll a : b ratio, lower photosynthetic rates
under dim light, higher maximum photosynthetic rate, higher stomatal conductance, and lower leaf internal CO
#
concentrations compared with those grown in either gap edge or gap centre (cloudy) regimes. Responses to the gap
edge Šs. gap centre (cloudy) treatments differ little, suggesting that shade acclimation in forest maple seedlings is
mainly a response to light intensity rather than spectral quality. The ubiquitous and, except for leaf internal CO
#
concentration, highly significant interspecific variation in traits was broad-ranging and continuous. These results
suggest that (1) the responses to light quality found in shade intolerant herbaceous and woody species growing in
more open habitats may not have a selective advantage in seedlings of shade tolerant forest trees, and (2) the adaptive
plastic response to understorey Šs. gap environments in forest maples, which is qualitatively consistent across species,
is founded on co-ordinated, small shifts in sets of functionally inter-related traits.
# 1998 Annals of Botany Company
Key words : Acer, forest gap heterogeneity, plasticity, specific leaf mass, photosynthesis, leaf chlorophyll, nitrogen,
stomatal density, root growth, root : shoot ratio, growth form.
INTRODUCTION
The importance of treefall gaps and similar disturbances in
the forest canopy for the growth, survival and reproduction
of species of Acer (Canham, 1985, 1988 ; Peters et al., 1995)
and many other tree seedlings is widely appreciated (Pickett
and White, 1985 ; Attiwill, 1994). Under an intact forest
canopy, maple saplings experience persistently low levels of
diffuse and spectrally altered sunlight (Messier and
Bellefleur, 1988 ; St. Jacques and Bellefleur, 1993) and are
only occasionally exposed to sunflecks (Chazdon and
Pearcy, 1991). Forest maples tolerate these shaded conditions as juveniles to varying degrees (Hoffmann, 1960 ;
Kurata, 1974 ; Burns and Honkala, 1990), but all depend on
the increased resources available in canopy gaps for their
longer term survival and reproduction (Wilson and Fischer,
1977 ; Hibbs, Wilson and Fischer, 1980 ; Canham, 1985,
1988 ; Fried, Tappeiner and Hibbs, 1988 ; Peters et al., 1995).
Interspecific differences in growth and survival of juvenile
maples growing in shaded Šs. more open environments
are tied to diverse plastic changes in morphological and
physiological traits (Ellsworth and Reich, 1992b ; Sipe and
Bazzaz, 1994, 1995 ; Walters and Reich, 1996 ; Lei et al.,
1996 ; Lei and Lechowicz, 1997 a, b). This paper concerns
the ecological and evolutionary significance of these plastic
responses to understorey Šs. gap environments, responses
that may or may not be adaptive (Lei and Lechowicz, 1990 ;
Sultan, 1992, 1995).
* Present address : Department of Biology, Virginia Tech.,
Blacksburg, VA 24061–0406. Fax 540 2319307, e-mail tomlei!vt.edu
0305-7364}98}070009­11 $30.00}0
While environmental plasticity is the norm, not the
exception, among plants, its ecological and evolutionary
significance remains a subject of debate (Sultan, 1992,
1995). Relatively few studies have considered whether such
phenotypic changes in traits across environments are
meaningful adaptive responses to environmental cues,
especially for forest trees (Sultan, 1992, 1995). Two aspects
of plastic responses by understorey tree seedlings to gap
formation are at issue. First, what are the environmental
cues that elicit and organize the plastic response. The
possible adaptive value of a response requires a consistent
relationship between a cue eliciting a plastic change and the
environment in which the new phenotype will grow. Second,
what is the functional significance of the response ? If a
plastic response does not contribute to more effective
physiological function or greater survival and reproduction
in the new environment, then the plasticity cannot be
considered adaptive (Sultan, 1992, 1995). This paper focuses
on the cues eliciting the plastic response of forest maples to
gaps in the forest canopy, and makes an initial assessment
of the adaptive significance of these responses.
The most striking environmental shift in a newly created
gap compared to the previously shaded understorey is in the
light regime, which is altered both quantitatively and
qualitatively. Understorey irradiance is typically only 1–5 %
of that at the forest canopy, and the red to far-red (R : FR)
ratio declines from the values of 1±0–1±2 typical of sunlight,
to only 0±1–0±5 (St. Jacques and Bellefleur, 1993 ; Turnbull
and Yates, 1993). Traditional views emphasize responses to
the quantitative changes in light regime following gap
formation (e.g. Bjo$ rkman, 1981), but recently there has also
bo980644
# 1998 Annals of Botany Company
10
Lei and Lechowicz—Plasticity of Forest Maples in Simulated Gaps
T     1. The Acer species inŠestigated with their contemporary assignments to sections (Šan Gelderen, de Jong and Oterdoom
1994) ; the species fall into three phylogenetic subgroups, which should be considered proŠisional pending assessment of the
rapidly accumulating molecular data : (a) RU, SA & GI, (b) PN, SP & RF, and (c) SR, NI, BU, MA & PL. Data on range,
stature at maturity and habitat collated from Hoffmann (1960), Kurata (1974), Burns and Honkala (1990) and Šan Gelderen,
de Jong and Oterdoom (1994). See Lei (1992) for seed source information
Acronym
SP
PN
RF
PL
MA
BU
SR
NI
RU
SA
GI
Species
Section
Stature (m)
Range
A. spicatum Lamarck
A. pensylŠanicum L.
A. rufinerŠe Sieb. & Zucc.
A. platanoides L.
A. macrophyllum Pursh.
A. buergerianum Miquel
A. saccharum Marshall
A. saccharum ssp. nigrum (Michx. f.)
Desmarais
A. rubrum L.
A. saccharinum L.
A. tataricum ssp. ginnala (Maxim.)
Wesmael
Parviflora
Macrantha
Macrantha
Platanoidea
Macrophylla
Pentaphylla
Acer
Acer
6
6–12
10–15
30
15–25
5–10
40
25
NE North America
NE North America
Japan
Europe
W North America
East Asia
NE North America
NE North America
Upland
Upland
Upland
Upland
Upland
Upland
Upland
Upland
30
40
5–6
NE North America
NE North America
Eurasia
Lowland and upland forests
Lowland forest
Upland forest
Rubra
Rubra
Ginnala
been considerable interest in tree responses to the qualitative
shift in the gap light regime (Kwesiga and Grace, 1986 ;
Kwesiga, Grace and Sandford, 1986 ; Warrington et al.,
1989 ; Riddoch, Lehto and Grace, 1991 ; Lee et al., 1996).
Irradiance alone may not be the only cue for the location of
a new gap as the R : FR ratio also varies somewhat
independently within and around the gap (Endler, 1993 ;
Turnbull and Yates, 1993). Furthermore, in some situations
such as coastal fog forest and montane cloud forest (e.g.
Vogelmann, 1973 ; Cavelier and Goldstein, 1989), young
maples will often be exposed to low photon flux density
(PPFD) but high R : FR similar to that of direct sunlight
(Gates, 1980). In these situations, and perhaps more
generally, R : FR may be a more reliable indication of
position in or near a gap than increase in light quantity. An
increased PPFD is ultimately an important cause of
accelerated growth in gaps, but an increased R : FR may
provide an essential stimulus to the coordinated physiological and morphological responses of shade-adapted
plants that allow their effective exploitation of a gap event.
We have therefore compared the responses of diverse maple
species to different combinations of PPFD and R : FR to
decide which environmental signals govern seedling
responses to gaps in the forest canopy.
Whatever the environmental cues for a particular plastic
response may be, an ancillary concern is the significance of
the morphological and physiological changes from one
environment to another. If a set of maples have differing
plastic responses, do those differences represent speciesspecific adaptations ? For example, does the shift in a trait
contribute to more effective physiological function in the
environment or demonstrably enhance survival or reproduction ? If a set of maples all show a similar plastic
response, is that response some sort of universal adaptation
or simply a reflection of a genetically fixed trait ? Interspecific
patterns of plastic responses mapped onto maple phylogeny
could reveal such a constraint on the evolution of adaptation
to forest light regimes. To begin answering such questions,
Habitat
forest
forest
forest
forest
forest
forest
forest
forest
we need to compare a fairly broad sample of forest maple
species grown in contrasting forest environments.
We grew seedlings of 11 species of forest maples under
three light regimes that simulated : (1) a forest gap centre
under clear skies ; (2) a gap edge ; and (3) a gap centre under
cloudy skies. The three light regimes were selected to
represent the range of light environments that forest maples
might encounter, and to separate the possible effects of light
quantity and light quality on the plastic responses of
seedlings. The sampled maples (Table 1) originate from
three continents, represent the major lines of phylogenetic
divergence within this well defined genus (van Gelderen, de
Jong and Oterdoom, 1994), and differ in their heights at
maturity and associated reproductive ecology (Hoffmann,
1960 ; Kurata, 1974 ; Burns and Honkala, 1990). Their
diversity provides a test of the generality of earlier
comparisons among maple species (Lei and Lechowicz,
1990, 1997 a, b ; Sipe and Bazzaz, 1994, 1995) and an
opportunity for an initial assessment of the ecological and
evolutionary significance of plastic responses to contrasting
forest light regimes.
MATERIALS AND METHODS
The 2- or 3-year-old seedlings of 11 Acer species used in the
experiment (Table 1) were raised from seed in the McGill
University Phytotron. The glasshouse compartment where
the seedlings were grown was programmed to track outdoor
conditions, except that in winter air temperature was held
just above freezing ; insolation was reduced throughout the
year with 50 % neutral density shade cloth. Seedlings were
grown in cylindrical Plexiglas ‘ rhizotrons ’ (61 cm deep ;
volume 2±8 l) filled with commercial top soil (Fafard et
Fre! res Lte! e, St. Guillaume, Que! bec, Canada) and covered
with an opaque plastic wrapping that could be removed to
assay root characters. The seedlings were watered as
necessary and fertilized weekly during the growing season
Lei and Lechowicz—Plasticity of Forest Maples in Simulated Gaps
with Hoagland’s solution (Dunn and Arditti, 1968, Version
2). In early spring (April) 1990, the seedlings were transferred
to a lath house at the university’s Mont St. Hilaire Research
Centre (45° 33« N, 73° 09« W) where leafing out took place
in the gap centre (clear), gap centre (cloudy) and gap edge
treatments described below. The seedlings were randomly
assigned to the three light treatments. Leaf morphology in
Acer is strongly determined by irradiance level during leaf
expansion (Isanogle, 1994 ; Goulet and Bellefleur, 1986)
and, unlike Fagus (Eschrich, Burchart and Essiamah, 1989),
little affected by light regime during development of leaf
primordia the preceding season ; we therefore expect the
influence of the experimental light regimes to dominate the
seedling responses. There was minimum shading from
neighbouring plants. During the experiment, seedlings were
fertilized once a week, and watered regularly. All plants
were harvested late in September 1990 as the normal
growing season ended.
Experimental design and light treatments
Three treatments were selected to approximate the
contrasting combinations of light quality and quantity
found in the centre of forest gaps under clear and under
cloudy skies, and at the edge of gaps under clear skies (Lee,
1987 ; Messier and Bellefleur, 1988 ; Canham et al., 1990 ;
Lawton, 1990 ; St. Jacques and Bellefleur, 1993 ; Turnbull
and Yates, 1993 ; Endler, 1993). The gap centre (clear)
treatment simulated the light regimes in a moderate size
(approx. 10 m diameter) forest gap ; plants were grown in a
lath house, which had 37 % open area in a latticed pattern, at
a lath to plant distance sufficient (Yates, 1989) to yield fairly
uniform irradiance at about 20 % open sky values and a
red to far-red ratio (R : FR) of 1±10. The forest edge light
regime was simulated by covering the lath roof and sides to
1 m from the ground with a spectral filter ; the lowest metre
of the compartment was shielded with 32 % transmittance
shade cloth (Les Industries Harnois Inc., St-Thomas-deJoliette, Que! bec, Canada). The spectral filter consisted of
alternating strips of filter pigments (17 cm) and clear (2±5 cm)
bands on polyurethane sheet (CIL Durafilm 1, from Les
Industries Harnois Inc. Que! bec, Canada). The banding
pattern, perpendicular to the solar track, created alternating
sunflecks and shade lasting 2 and 13 min, respectively. The
filter pigment mixture follows Lee (1985) but without the
carbon black. This arrangement yielded a gap edge regime
with about 2±5 % open sky irradiance and a R : FR of 0±60,
occasionally punctuated by simulated sunflecks with higher
irradiance and R : FR ratio. The gap centre (cloudy)
treatment was designed to simulate the natural light
properties of low PPFD and high R : FR prevailing during
continuous cloud cover or fog (Gates, 1980). It consisted of
10 % transmittance shade cloth on the roof (without lath)
and 17 % transmittance shade cloth on all four sides.
Irradiance under this treatment was about 1±5 % of open sky
but R : FR was 1±03. This treatment allows an evaluation of
any independent effects of light quality and quantity on
Acer seedlings by comparison to the gap centre (clear) and
cloudy regimes.
11
Light chamber design for gas exchange determination
Photosynthesis, leaf internal CO and stomatal conduc#
tance were measured twice on each plant with a LiCor 6200
Portable Photosynthesis System (Lincoln, Nebraska, USA)
on 23–30 Jul., 1990. Both dynamic and steady-state gas
exchange measurements were made under artificial lights in
the Mont St. Hilaire Research Centre near the lath house.
Plants were brought inside (by random block and treatment)
and acclimated for at least 1 h under an array of fluorescent
tubes and incandescent bulbs, giving a mean PPFD of
29 µmol m−# s−" and R : FR of 0±95. After acclimation, gas
exchange was measured under this dim light on one
randomly selected leaf per plant. Seedlings were then moved
under a GE Cool Beam Flood Lamp (300W PAR 56}2MFL)
suspended over a thermal barrier ; mean PPFD was
1260 µmol m−# s−" and R : FR was 1±90. Gas exchange of the
same leaf measured under dim light was determined after
0±5 min and 24±5 min of exposure to this bright light. This
procedure simulates the initial stage (at 0±5 min) and steady
state (at 24±5 min) photosynthetic inductive response of a
dim-light-acclimated leaf to a saturating sunfleck. Photosynthesis at 24±5 min is referred to as Amax, based on
preliminary determinations that the seedling response curves
began to plateau at approx. 10 min in all the Acer
species. Repeated handling of the same leaf at these time
intervals had no affect on gas exchange characteristics.
Plant characters
In June 1990, fine root (! 2 mm diameter) density was
estimated by counting the number of fine roots intercepted
along six circumferences (24 cm each) of the ‘ rhizotron ’ at
5, 8, 26, 29, 47 and 50 cm depths. A record of the root
positions along the transects was kept on an acetate sheet
and 1 month later a second census was taken at the same
positions. Fine root density was estimated as the number of
roots intercepting the six transect lines, and is expressed as
number of fine roots per cm. Mean fine root density of two
censuses (July and August) is reported. Acer root growth
is maintained at a steady rate from June to senescence
(Millard and Proe, 1991) and root production rates determined in this study are representative of summer belowground growth activities.
On 22–23 Sep. 1990, abaxial leaf (Acer is a hypostomatous
genus ; Powers, 1967) impressions were made with clear nail
polish for stomatal density and pore diameter measurements
(Lei and Lechowicz, 1990). Impressions were taken from
three randomly chosen leaves per plant. We made three
stomatal density counts and four stomatal pore diameter
measurements per impression. Immediately after leaf impressions were collected, all leaves from each plant were
harvested. A random subsample of ten discs (each 20 mm#)
from five leaves was used to determine specific leaf mass
(SLM) ; the remaining tissue was kept in a ®18 °C freezer
for subsequent chlorophyll determination. A LiCor Area
Meter (Li-3100) was used to measure total leaf area on each
seedling. Lengths and number of shoots on each plant were
recorded. Leaf, twig and roots were separated and oven-
12
Lei and Lechowicz—Plasticity of Forest Maples in Simulated Gaps
Treat
***
A
SP
***
T*S
NS
C
LDI-wt-based (cm–2 g–1)
***
BU
***
20
PL
PN
SA SP
MA SR
RU
16
RF
BU
GI
12
8
NI
PL
SP MA
RU
RF SR
SA
BU
PN
GI
SP
RU PL
MA
PN
SR RF
BU
GI
SA
0.6
***
***
0.6
0.5
0.4
0.3
0.2
NI
MA
SR
MA
PL
BU SP
SP
RF PL GI
RU SA
BU
PN
RU
0.4
RU
PL
NI
0.2 PN
BU MA GI
NI SP RF
SR PN SA
PL
RF
MA
SP BU GI PN
SR SA NI
SR
D
***
500
***
*
NI
SP
BU
400
300 SR
200
***
SP
NI
SA
BU
SR
NI PN
BU SP
PN
RF GI
PL MA
RU SA
SA
PL GI
GI
RF RU
PN SA
1.8
F
SA PN
GI
RU RF
MA PL
***
***
*
***
*
BU
1.4
1
0.6
GI
SP
MA RF
SA
PN
SR
RU
PL
NI
BU MA
GI
SR NI
RF
SP RU
PN
SA PL
0.2
Clear
G
BU MA
GI
RU
PL NI SP
RF SR
SA
PN
Cloudy
Gap centre
Gap edge
SP
SA BU
PN
RF
MA
SP
GI
NI SR
SP
BU
MA RF
RU SR
PL NI
SA GI
PN
PL
RU
0.1
0
0.6
RU
SA
GI
SP RF
MA
0
NS
SRNI
SR SP
PL MA
GI
SA
RF BU
PN
0.2
0.7
PL
0.8 BU
RF RU
100 MA
1.8 NI
1
1
*
NI
E
RGR plant ht (cm cm–1 yr)
MA
SA SR PN
SP RF
24
1.4
T*S
*
NI
4
RGR basal dia (mm mm–1 yr)
PL
RU
SR
PN
SA
MA
SP RF
BU
PN SP
BU
RF
RU
Fine root density (cm–1)
NI
0.2
28
GI
NI
PL
LDI-len-based (cm2 cm–1)
0.4
GI
NI MA
SR
PL RU
SA
RGR twig len (cm cm–1 yr)
Root:shoot ratio
1
0.6
SP
***
RU
1.2 GI
0.8
1.2
Treat
***
B
NI BU
RF
SR
SA
PN
GI MA
PL RU
Cloudy
Clear
Gap centre
Gap edge
F. 1. Norm of reaction diagrams and associated ANOVA results summarizing responses of the different species of Acer seedlings grown under
three light regimes (see Methods). This figure summarizes responses related to the growth and architecture of the seedlings. Lines connect the mean
response of each species to the three contrasting light regimes ; note that the x-axis is ordinal, the y-axis quantitative. The species acronyms are
given in Table 1. Trait abbreviations : Fig. 1 C, Shoot dry weight-based Leaf Display Index ; D, shoot length-based Leaf Display Index ; E, relative
growth rate of vertical plant height ; F, RGR of total twig length. ANOVA results appear above each graph : Treat, treatment main effect ; Sp,
species main effect ; T*S, treatment by species interaction ; NS, no significant difference ; *P ! 0±05 ; ** P ! 0±01 ; *** P ! 0±001.
13
Lei and Lechowicz—Plasticity of Forest Maples in Simulated Gaps
Treat
***
A
5
0.26
GL
PL
RFRU
BU
SA
NI SP
MA
MA
RU GI
MA
PL
BU
RF
SP SA RU
NI SR
PN
RF PL
SA NI BU
SP
SR
PN
PN
SR
3
1
***
MA
RU
1
Adim (µ mol/m–2 s–1)
***
BU
0.8
RU
SA SP
0.6
PL
NI GIPN SR
0.4
MA
NS
PL
SR BU GI SP
PN NI
RF
SA
MA BU
SP PN
SA
PL
NI
RU SA
RF
0
RF
0.14
PLRF
BURU
0.1 SA SP
NI
PN SR
0.06
MA
RU GI
SA BU
RF PL NI
SP
SR
PN
GI
PL BU
SP RF SA
RU
SRNI
PN
D
***
***
0.1 GI
RF
0.08
0.06
***
NS
NS
80
BU
300
280
GI MA RU
PL
SP
SR PN RF
SR
RF
SP
PN MA
PL SA
BU GI NI
RU
Clear
Cloudy
Gap centre
SP RU
SA
MA
NI BU GI
PL
SR
PN SF
Pn induction (%) at 30 s
SANI
70
SP SA
NI
RU
SR
PL
BU
PN
MA
RU
SP SA GI
RF PL NI BU
SASPSR
BU GI PL
RF
NI
RU
PN
SR
PN
***
SR
NI
50
SA SP
GI
30 PN BU RU
MA
RF
PL
20
Gap edge
F
60
40
NS
MA
0.12
0.02
E
Ci at Amax (ppm)
GI
0.04
–0.2
220
MA
0.18
MA
GI
0.2
–0.4
T*S
NS
0.22
0.14
gs at Adim (mol m–2 s–1)
C
240
SP
***
0.02
1.2
260
Treat
***
B
MA
MA
9
7
T*S
NS
gs at Amax (mol m–2 s–1)
Amax (µ mol/m–2 s–1)
11
SP
***
SRSP
NI
RU
SA
PL
MA
GI PN
RF
BU
Clear
Cloudy
Gap centre
***
NS
SR
NI
SP
PL
SA
MA
RF
BU PN
GI
RU
Gap edge
F. 2. Norm of reaction diagrams and associated ANOVA results summarizing responses of the different species of Acer seedlings grown under
the three light regimes : responses in traits related to gas exchange. The format and coding of the diagrams are given in the caption to Fig. 1.
dried for biomass determination. Plant height and basal
diameter were measured in May and again in September.
Chlorophyll a and b levels were determined on freshly
frozen leaves (one pooled sample per tree) using a DMSO
extraction method adapted from Barnes et al. (1992).
Chlorophyll levels were estimated from absorption values
using formulae for 80 % Acetone in Barnes et al. (1992). No
chlorophyll degradation products were evident during this
procedure. Leaf N was determined by a Kjeldahl analysis
(Bradstreet, 1965) using a pooled sample of oven-dried
(70 °C) leaves for each plant. Ground leaf samples (0±100 g
each) were digested for approx. 90 min with six selenium
catalyst granules, 0±5 g K SO and 5 ml concentrated H SO ;
# %
# %
the digest was Nesslerized and assayed colorimetrically
14
Lei and Lechowicz—Plasticity of Forest Maples in Simulated Gaps
Specific leaf mass (g m–2)
40
SP
***
T*S
NS
RUGI
PL
RFNI
MA
BUSR
36
32
GI
RF
GI
SA SP
PN
RFPL
MA
BUNIRU
SR
PN
SA
RU
MA
NI PL
SR
BU SA
28
24
PN
20
SP
Treat
***
B
Stomatal density (mm–2)
Treat
***
A
GI
BU RF
700
500
300
SP
***
T*S
NS
GI
RF
GI
RF
BU
NI
PL SP
MA PN
RU SA
SR
BU RU
RU
SR PL SN
NIMA PN
SP
SP
PL SR
NI MA
SA
PN
SP
100
***
3.2
SA
GI
GI
***
***
NS
SR
1.1
0.9
GI NI
BU PLMA
PN
RF SA
RU
SP
0.7
RF
SR
MA RF
BU PL
GI
NI
PN
SA RU
SR
MA
NI
SA
GI
BU PL
RU
SP
0.5
E
***
***
*
7
SR
NI
GI
MA NI
PL
BU
PL
BU SR
MA
PN
SP RU
RF
SA
SP GI
RF
PN SARU
MA
BU
SP RF
GI RU
PN
F
***
6
5
SR
GI
SR
PN
PL
MA
BU
RF RU
SA
GI
RF PL MA
RU
BU PN
NI
NI
SA
SP
Clear
4
Cloudy
Gap centre
Gap edge
***
NS
SA
SR NI
PL
5
2.5
RU
D
PN
SP
5.5
3
PN
RF
SA
SP NI PL
RU
6
3.5
BU
BU
PL
PN
PN
MA
NI
2.4 BU GI
SA PL
2.2 SP
2 RF
RU
1.8
2.6
4
SR
MA
SP RF NI
2.8
4.5
1.3
MA
SR
3
***
Leaf nitrogen (g m–1)
SR
6.5
Total chlorophyll (mg g–1)
***
Chlorophyll a:b
Leaf nitrogen (%)
C
3.4
SP
Clear
SA
SR
PN GI
RF BU
NI
PUMA
PL
SP
Cloudy
Gap centre
Gap edge
F. 3. Norm of reaction diagrams and associated ANOVA results summarizing responses of the different species of Acer seedlings grown under
the three light regimes : responses in traits related to the structure and composition of leaves. The format and coding of the diagrams are given
in the caption to Fig. 1.
(Middleton, 1960). Regular checks of the assay method
using US National Bureau of Standards apple leaf samples
showed high repeatability and good accuracy.
Statistical methods
The total number of seedlings used in the experiment was
168 (four replicates per species-population per treatment).
The experimental plants were arranged in four blocks in
each light treatment, one seedling per species-population
per block. Differences between light treatments, species and
treatment by species interaction were analysed using
Procedure GLM in SAS (1989) for a two-factor fixed effects
model. ANOVA showed no significant block effect in the
traits measured and block effects will not be considered in
subsequent analyses. The s.e. associated with data presented
Lei and Lechowicz—Plasticity of Forest Maples in Simulated Gaps
in Figs 1–3 was in the order of 5–15 % of the mean.
Readers wanting more quantitative detail on the patterns
reported in these summary figures are invited to request the
full data set from the authors.
RESULTS
For all the diverse traits that we investigated, there were
significant differences among the various maple species in
their response to the three combinations of light quantity
and quality (Figs 1–3). The species responses generally fall
on a continuum of greater or lesser range, occasionally with
one or two slightly more extreme responses (compare, for
example, Fig. 2 A and C). Many traits showed significantly
different responses to the three experimental light regimes,
but these differences were most often founded on light
quantity [between gap centre (clear) and gap edge], not light
quality (between gap edge and gap centre : cloudy) (cf. Figs
1 A, B, E, G ; 4 C, D ; 5 A, C, D–F). The nature of the
relationships among species sometimes changed across the
treatments ; in statistical terms, there were some significant
interactions between species and treatment responses (cf.
Figs 1 B–D, F, G ; 5 C, E). These interactions arise from
differences among treatments in the spread of species values
and}or changes in species ranks among the treatments. We
also analysed these traits with an additional growth form
factor (in ANOVA) which separates large tree (canopy
species) from small trees (subcanopy species), but found no
significant effect for all traits examined. We review the
noteworthy aspects of the individual responses in the
following paragraphs.
Shoot growth and plant structure
All the plants grown in gap centre (clear) had higher
root : shoot ratio and greater numbers of fine roots than
those grown in the two low PPFD environments (Fig. 1 A
and B). Root : shoot ratio was highest in A. ginnala, but this
singularity does not arise from unusually high root density
(Fig. 1 B). Acer rubrum has notably high root density in all
three light regimes.
Light regime had no effect on the display of leaves along
branches, despite substantial interspecific differences in this
measure of canopy architecture (Fig. 1 C). Acer nigrum
consistently had the greatest leaf area per unit branch length
and A. ginnala most often had the least. The woody tissue
invested in branch per unit leaf area shows a similar lack of
response to light regime, but in this instance there is also a
significant interaction between species and treatment (Fig.
1 D). This interaction arises from the tendency for only three
of the species (A. nigrum, A. spicatum, and A. buergerianum)
to increase the leaf area supported per unit branch wood.
Gap-grown plants showed marginally higher relative
growth rate (RGR) in vertical height, with the highest
growth rates found in the two closely related species of A.
saccharum and A. nigrum (Fig. 1 E). RGR in total twig
length shows a significant interaction between treatment
and species (Fig. 1 F). Those species that reach maturity as
part of the canopy crown (i.e. A. saccharum, A. macrophyllum, A. plantanoides and A. nigrum) maintained similar
twig growth in all three treatments, while those that mature
15
as subcanopy or small trees (i.e. A. buergerianum, A.
ginnala, A. spicatum, A. rufinerŠe and A. pensylŠanicum)
exhibit a substantial decrease in growth from gap centre
(clear) to the two low PPFD treatments. The lack of
discernible variation in twig growth between gap edge and
gap centre (cloudy) treatments in all species indicates that
R : FR has little effect on growth rates. The RGR in stem
basal diameter of all species showed an increase in basal
diameter growth under the gap treatment. However, the
relative growth rates were not separated as species of
different growth forms.
Gas exchange
Both photosynthesis (A) and stomatal (gs) conductance
under saturating light (Amax and gs at Amax respectively)
showed strong PPFD-dependent patterns for all species
(Fig. 2 A and B). In these two gas exchange traits, the
similarity between gap edge and gap centre (cloudy) indicates
a lack of light quality effect. The obvious exception was
A. macrophyllum, where A and gs measured under both
saturating and dim light were the highest among the species
in all three treatments. The large drop in both gs and A by
A. macrophyllum in the gap centre (cloudy) treatment (Fig.
2 A, B, D) suggests that the photosynthetic capacity of this
coastal Pacific species can respond to variations in R : FR
light alone. It is interesting that A. macrophyllum, which is
the only sampled species that frequently occurs in foggy
coastal forests, is the only species to show a marked
difference in response to overcast Šs. shaded growth regimes.
In all species, variation in gs at Amax is strongly correlated
with Amax under the three treatments (Fig. 2 A and B), but
the coupling between these two traits is not apparent under
dim light (Fig. 2 C and D). A. rufinerŠe appears to be
particularly poor in dim light photosynthesis, perhaps due
to unusually high dark respiration rates. A. pensylŠanicum
and A. saccharum showed consistently low gas exchange
performance in all three treatments under both saturating
and dim light conditions (Fig. 2 A–D).
The leaf internal CO at Amax (Ci) of plants grown in gap
#
centre (cloudy) was higher than those in gap centre (clear)
and gap edge light regimes. The similarity between the latter
two regimes where PPFD and R : FR were both high [gap
centre (clear)] or both low (gap edge) suggest an effect of an
interaction (i.e. low PPFD and high R : FR ratio) on leaf
internal CO . In the gap centre (clear) treatment, seven of 12
#
species had a Ci between 230 and 265 ppm. This could be
the range of stable CO partial pressure which all species
#
maintain through stomatal regulation under saturating light
conditions. The high Ci and low Amax in A. saccharum
suggests a relatively ineffective conversion of light energy to
carbon uptake in this species. At the other extreme, A.
pensylŠanicum was notably conservative in managing its gas
exchange with low gs and modest Amax associated with low
Ci. This is the only trait among those examined with no
significant differences among species.
The maple species differ significantly in the speed with
which they attain steady state photosynthesis when exposed
to high irradiance, but these differences do not depend on
light regime (Fig. 2 F). Photosynthetic induction rate is
16
Lei and Lechowicz—Plasticity of Forest Maples in Simulated Gaps
calculated as the percent ratio of transient photosynthesis
after a 30 s exposure to saturating light : steady state rate
(after 24±5 min). Higher values, such as in A. saccharum,
may be interpreted as a more rapid response to the onset of
sunflecks in shade-acclimated plants (Chazdon and Pearcy
1985, but see Lei and Lechowicz, 1997 a). Photosynthetic
induction appears not to be strongly correlated with Amax,
since both A. macrophyllum (high Amax) and A. pensylŠanicum (low Amax) showed low rates of induction (Fig.
2 A, F).
Leaf structure and composition
There were significant differences in specific leaf mass
(SLM) among the maples, and all the maples had greater
SLM when grown in the gap centre (clear) regime compared
to gap edge or gap centre (cloudy) (Fig. 3 A). Acer ginnala
had notably high SLM in all growth regimes, and A.
spicatum had especially low SLM in the two low PPFD
regimes.
There were significant differences among the maples in
their weight-based leaf nitrogen concentrations with lower
concentrations in plants grown in gap centre (clear)
compared to those in gap edge or gap centre (cloudy) (Fig.
3 C). Acer saccharum has extremely high leaf nitrogen
concentrations and A. rubrum notably low concentrations.
These concentration data can be converted to an estimate of
areal investments in nitrogen by combining with SLM data
for each seedling (Fig. 3 D). The high investment in leaf
nitrogen by A. saccharum then remains clear on an areal
basis, but a notably low investment by A. spicatum also
becomes apparent.
Leaf chlorophyll concentration varied significantly among
treatments and among species (Fig. 3 E). Most species
showed an increase in chlorophyll level with decreasing
PPFD [i.e. from gap centre (clear) to gap edge], with A.
ginnala being the exception. There was also a tendency for
chlorophyll level to peak at the gap edge regime where
R : FR was lower than the other two treatments. The ratio of
chlorophyll a to chlorophyll b decreased from high PPFD to
low PPFD treatments and showed significant differences
among species (Fig. 3 F). Acer saccharinum and A. saccharum
have fairly high chlorophyll a : b ratios and A. spicatum has
a consistently low chlorophyll a : b ratio.
Finally, there are substantial interspecific differences and
treatment effects in stomatal density (Fig. 3 B). Except for
A. saccharum and A. rubrum, stomatal density decreases
from gap centre (clear) to gap edge-grown plants. The three
Asian species : A. ginnala, A. rufinerŠe and A. buergerianum
have consistently high stomatal density and A. spicatum,
along with low SLM, tends also to have low stomatal
density.
DISCUSSION
Forest maples respond primarily to changes in light quantity
associated with canopy gaps, and most traits do not respond
to concordant changes in light quality. All forest maples
show essentially the same responses to low irradiance,
regardless of whether the R : FR ratio is characteristic of
open sky or gap values. The canopy species, whose
maturation is so strongly dependent on release growth
during gap events (Canham, 1985, 1988 ; Fried et al., 1988 ;
Peters et al., 1995), do not show any greater sensitivity to
the increase in R : FR than subcanopy species. This general
indifference of forest maples to R : FR levels existing within
and around canopy gaps is true for a variety of morphological, biochemical and physiological traits, including
measures of growth. Studies of tropical tree seedlings show
a comparable lack of sensitivity to light quality for shade
tolerant species (Kwesiga and Grace, 1986 ; Lee et al., 1996).
Given the well-documented responses of shade intolerant
trees to light quality as well as quantity (Kwesiga and
Grace, 1986 ; Warrington et al., 1989 ; Lee et al., 1996), some
of the more ruderal maples like A. negundo (Maeglin and
Ohmann, 1973) and A. campestre (Ku$ ppers, 1984) may
respond to changing R : FR ratio under high irradiance. In
general though the forest maples respond primarily to the
quantitative increases in irradiance associated with gap light
patches and not to any associated changes in R : FR ratio.
The sole importance of quantitative changes in irradiance
does not preclude the possibility for adaptive, interspecific
differences in response to gaps among maple species.
Quantitative variation in the light regime within gaps, which
has been recognized by earlier authors (e.g. Runkle, 1985 ;
Canham, 1988 ; Wayne and Bazzaz, 1993 a, b), is complex
and substantial. Over a 5-m distance in a gap from edge to
centre and from the forest floor towards the crown, both
direct-beam and diffuse irradiance typically differ more
than five-fold (Nakashizuka, 1985 ; Canham et al., 1990 ;
Lawton, 1990). Such gradients extend beyond the limits of
the vertical projection of the gap itself and can influence
seedlings growing in the adjacent understorey. While PPFD
decreases with increasing clouds, light intensity may remain
the same or even increase from gap edge to the closed forest
(Endler, 1993 ; Lei et al., 1998) due to stronger diffused
radiation. Within a gap, the seasonal and daily tracks of the
sun cast a gradation of direct beams (i.e. sunflecks of
different intensities and durations) through the gap into the
adjacent forest. The gradient of PPFD between gap centre
and closed canopy is also enhanced by differences in forest
structure. For example, in more open woodlands with large
areas of open sky not in the path of direct sunlight, the
contrast between gap and closed canopy conditions blurs
(Endler, 1993). Endler’s comments on the nature of
woodland shade also apply to places where topography (e.g.
north-facing slopes, stream bank), substrate (shallow, poor
or flooded soils) or exposure (ridgetops) reduce the density
or height of forest canopy and increase the amount of open
sky. These effects of weather, topography, forest density,
gap geometry and solar movement create a spatially
heterogeneous light regime around a canopy gap
(Lieberman, Lieberman and Peralta, 1989 ; Canham et al.,
1990 ; Runkle, 1990), with consequent effects on the spatial
distribution and growth of sapling trees (Wayne and Bazzaz,
1993 a, b ; Sipe and Bazzaz, 1994, 1995). All these sources of
variation within and among gap environments provide
ample opportunity for the ecological and evolutionary
diversification of forest maples on gap-related environmental gradients (Lei and Lechowicz, 1990 ; Sipe and
Bazzaz, 1994, 1995).
Lei and Lechowicz—Plasticity of Forest Maples in Simulated Gaps
While forest maple species do differ significantly in their
responses to light regime (Sipe and Bazzaz, 1994, 1995 ; Lei
and Lechowicz, 1997 a, b), these differences do not fall
into neat ecological or evolutionary categories. Although
the 11 species investigated had distinctive morphological,
biochemical and physiological characteristics (Figs 1–3),
these were not tied to species differences in size at maturity
(Table 1) as we expected initially (Lei and Lechowicz,
1990). For example, a canopy species like A. saccharum
has gas exchange characteristics more like the subcanopy.
A. pensylŠanicum than another canopy species, A. macrophyllum. In terms of seedling growth and demography,
juvenile Acer macrophyllum, which is a large canopy tree
at maturity, also behaves more like the subcanopy species
A. pensylŠanicum (Wilson and Fischer, 1977 ; Hibbs et al.,
1980 ; Fried et al., 1988) than like canopy species such as
A. saccharum or A. mono (Canham, 1985, 1988 ; Peters et al.,
1995). Nor do these complicated patterns of interspecific
variation fall on phylogenetic lines, at least not by our
present understanding of phylogenetic relationships within
Acer (cf. Table 1 ; van Gelderen et al., 1994). Acer saccharum
and A. macrophyllum are closely related, yet have strongly
contrasting morphological and physiological characteristics.
In other words, the pattern of interspecific variation in these
forest maples defies simple categorization. The different
characteristics of each species fall on continuous quantitative
gradients of variation, not into qualitatively distinct subsets
on ecological or phylogenetic lines. Some of this continuous
variation may be related to specialized adaptation to
contrasting forest environments, but we cannot be certain as
the ecology of these species is too poorly quantified.
The general functional value of many of the plastic
responses that are consistent among these forest maple
species is more straightforward. For example, although
levels of total chlorophyll differ among the studied species,
the plastic response in total chlorophyll is consistent and
functionally sensible. Total chlorophyll levels increase for
all these forest maples when seedlings are grown at low
irradiance, as we would expect given the role of increased
chlorophyll content in improving light harvesting capacity
in the shade (Chow et al., 1990 a, b). Similarly, the
chlorophyll a : b ratio is lower for all the maples in low light
regimes (Fig. 3 F), which is consistent with the expected
greater investment in chlorophyll b to enhance photosystem
II function under low irradiance (Lei et al., 1996). Most
maple species showed no indication of altering chlorophyll
investment in response to light quality alone (i.e. gap centre
cloudy Šs. gap edge, Fig. 3 E and F). This lack of response
to light quality in regulation of chlorophyll investment is
consistent with reports for tropical tree seedlings of different
successional status (Turnbull, 1991) and tropical vines (Lee,
1988). It is noteworthy that there is a suggestion of a
qualitative response in some of the canopy maples : A.
saccharum, A. nigrum and A. plantanoides (cf. Fig. 3 E and
F). In general though, the plastic response of chlorophyll
to light regime follows the same pattern regardless of interspecific differences in the amount of chlorophyll.
We can note other examples of a generalized adaptive
response in all these maples to low Šs. high irradiance
growth regimes. Gap-grown plants consistently have a
17
higher root : shoot ratio and a greater density of fine roots
(Fig. 2 A and B), which is consistent with the greater
evaporative demand characteristic of the sunnier gap
environment. The greater photosynthetic capacity (Fig. 1 A)
and associated nitrogen investments (Fig. 3 D) of leaves
from the sunny gap environment is commensurate with the
higher irradiance in the sunny gap. On the other hand,
adaptation to the shaded regimes is less certain (Fig. 1 C
and F ; Lei and Lechowicz, 1997 a). It should be noted here
that some of the treatment effects on whole plant characters
may have been dampened by the growth environment prior
to the experiment, but the overall patterns of responses
should prevail, even if a second year of treatments were
imposed. What remains interesting is the quantitative
variation among these maple species, despite the frequent
qualitative similarity of their responses to contrasting
growth regimes. The challenge is to identify the functional
basis for the interspecific differences in traits and their
plastic responses for the many other traits that we know to
be important to seedling growth and survival in forest trees.
Efforts have been made to relate patterns of variation
in functionally important traits to plant performance in
herbs (Farris and Lechowicz, 1990) and also in trees
(Atipanumpai, 1989 ; Ceulemans, 1990). These investigations suggest that, as would be expected, intraspecific
variation in a given trait is usually functionally co-ordinated
with variation in other traits. Selection does not work on
traits in isolation, as known to both plant breeders and
evolutionary ecologists. The continuous variation evident in
all the traits we have compared here across different species
of Acer suggest that similar patterns of co-ordination
among traits can prevail at the generic level. It appears that
there is an underlying template that organizes variation
among traits in forest maples, but that within the constraints
of that template species can find individualistic combinations
of traits that are functionally viable and perhaps better
suited to one or another environment. Such co-ordinated
and constrained variation in a set of functionally interrelated
traits may be the basis for ecological differentiation among
forest maple species.
A C K N O W L E D G E M E N TS
Field and laboratory assistance was provided by Maria
Murgante, Maria Fernandes, Christian Piche! , Lucie
Veillette, Ste! phane Dumont and especially Rebecca Ritchie.
We thank the Gault Estate Board of Directors for permission
to work at the Mont St. Hilaire reserve. Pierre Bellefleur
kindly lent a Li-3100 spectroradiometer. We thank Michel
Drew, Graham Bell and Jean-Pierre Charbonneau for
providing logistical support at the field site. Partial funding
in support of this study was provided by the Bourses
Que! bec-Re! publique Populaire de Chine and the Arthur
Willey Memorial Fellowship (McGill University) to TTL,
and by NSERC grant funds to MJL.
LITERATURE CITED
Atipanumpai L. 1989. Acacia mangium : studies on the genetic Šariation
in ecological and physiological characteristics of a fast-growing
18
Lei and Lechowicz—Plasticity of Forest Maples in Simulated Gaps
plantation tree species. Helsinki : The Finnish Forest Research
Institute.
Attiwill PM. 1994. The disturbance of forest ecosystems : the ecological
basis for conservative management. Forest Ecology and Management 63 : 247–300.
Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW. 1992. A
reappraisal of the use of DMSO for the extraction and
determination of chlorophylls a and b in lichens and higher plants.
EnŠironmental and Experimental Botany 32 : 85–100.
Bjo$ rkman O. 1981. Responses to different quantum flux densities. In :
Lange OL, Nobel PS, Osmond CB, Ziegler H, eds. Plant
physiological ecology I. (Encyclopedia of plant physiology, Šolume
12A). Berlin : Springer-Verlag, 57–107.
Bradstreet RB. 1965. The Kjeldahl method for organic nitrogen. New
York : Academic Press.
Burns RM, Honkala BH. 1990. SilŠics of North America. Volume 2.
Hardwoods, United States Department of Agriculture. Agricultural
Handbook 654. Washington DC : Forest Service.
Canham CD. 1985. Suppression and release during canopy recruitment
in Acer saccharum. Bulletin of the Torrey Botanical Club 112 :
134–145.
Canham CD. 1988. Growth and canopy architecture of shade-tolerant
trees : response to canopy gaps. Ecology 69 : 786–795.
Canham CD, Denslow JS, Platt WJ, Runkle JR, Spies TA, White PS.
1990. Light regimes beneath closed canopies and tree-fall gaps in
temperate and tropical forests. Canadian Journal of Forest Research
20 : 620–631.
Cavelier J, Goldstein G. 1989. Mist and fog interception in elfin cloud
forests in Colombia and Venezuela. Journal of Tropical Ecology 5 :
309–322.
Ceulemans R. 1990. Genetic Šariation in functional and structural
productiŠity determinants in poplar. Amsterdam : Department of
Biology, University of Antwerp.
Chazdon RL, Pearcy RW. 1991. The importance of sunflecks for forest
understorey plants. Bioscience 41 : 760–766.
Chow WS, Anderson JM, Melis A. 1990 a. The photosystem stoichiometry in thylakoids of some Australian shade-adapted plant
species. Australian Journal of Plant Physiology 17 : 665–674.
Chow WS, Anderson JM, Melis A. 1990 b. Adjustments of photosystem
stoichiometry in chloroplasts improve the quantum efficiency of
photosynthesis. Proceedings of the National Academy of Science
87 : 7502–7506.
Dunn A, Arditti J. 1968. Experimental physiology. Experiments in
cellular, general and plant physiology. New York : Holt, Rinehart
and Winston.
Ellsworth DS, Reich PB. 1992 a. Water relations and gas exchange of
Acer saccharum seedlings in contrasting natural light and water
regimes. Tree Physiology 10 : 1–20.
Ellsworth DS, Reich PB. 1992 b. Leaf mass per area, nitrogen content
and photosynthetic carbon gain in Acer saccharum seedlings in
contrasting forest light environments. Functional Ecology 6 :
423–435.
Endler JA. 1993. The color of light in forests and its implications.
Ecological Monographs 63 : 1–27.
Eschrich W, Burchart R, Essiamah S. 1989. The induction of sun and
shade leaves of the European beech (Fagus sylŠatica L.) :
anatomical studies. Trees 3 : 1–10.
Farris MA, Lechowic MJ. 1990. Functional interactions among traits
that determine reproductive success in a native annual plant.
Ecology 71 : 548–557.
Fried JS, Tappeiner II JC, Hibbs DE. 1988. Bigleaf maple seedling
establishment and early growth in Douglas-fir forests. Canadian
Journal of Forest Research 18 : 1126–1233.
Gates DM. 1980. Biophysical ecology. Berlin : Springer-Verlag.
van Gelderen DM, deJong PC, Oterdoom J. 1994. Maples of the world.
Portland OR : Timber Press.
Goulet F, Bellefleur P. 1986. Leaf morphology plasticity in response to
light environment in deciduous tree species and its implication on
forest succession. Canadian Journal of Forest Research 16 :
1192–1195.
Hibbs DE, Wilson BF, Fischer BC. 1980. Habitat requirements and
growth of striped maple (Acer pensylŠanicum L.). Ecology 61 :
490–496.
Hoffmann E. 1960. Der Ahorn : Wald-, Park- und Strassenbaum. Berlin :
VEB Deutscher Landwirdschaftsverlag.
Isanogle IT. 1944. Effects of controlled shading on the development of
leaf structure on two deciduous tree species. Ecology 25 : 404–413.
Ku$ ppers M. 1984. Carbon relations and competition between woody
species in a central European hedgerow. I. Photosynthetic
characteristics. Oecologia 64 : 332–343.
Kurata S. 1974. Illustrated important forest trees of Japan. 2nd edition.
Tokyo : Chikyusha.
Kwesiga FR, Grace J. 1986. The role of the red}far-red ratio in the
response of tropical tree seedlings to shade. Annals of Botany 57 :
283–290.
Kwesiga FR, Grace J, Sandford AP. 1986. Some photosynthetic
characteristics of tropical timber trees as affected by the light
regime during growth. Annals of Botany 58 : 23–32.
Lawton RO. 1990. Canopy gaps and light penetration into a windexposed tropical lower montane rain forest. Canadian Journal of
Forest Research 20 : 659–667.
Lee DW. 1985. Duplication of foliage shade for research on plant
development. HortScience 20 : 116–118.
Lee DW. 1987. The spectral distribution of radiation in two neotropical
rainforests. Biotropica 19 : 161–166.
Lee DW. 1988. Simulating forest shade to study the developmental
ecology of tropical plants : juvenile growth in three vines in India.
Journal of Tropical Ecology 4 : 281–292.
Lee DW, Baskaran K, Mansor M, Mohamad H, Yap SK. 1996.
Irradiance and spectral quality affect Asian tropical rain forest tree
seedling development Ecology 77 : 568–580.
Lei TT. 1992. Functional design and shade adaptation in Acer species.
Ph.D. Thesis. Montre! al, Que! bec, Canada : Department of Biology,
McGill University.
Lei TT, Lechowicz MJ. 1990. Shade adaptation and shade tolerance
in saplings of three Acer species from eastern North America.
Oecologia 84 : 224–228.
Lei TT, Lechowicz MJ. 1997 a. The photosynthetic response of eight
species of Acer to simulated light regimes from the centre and
edges of gaps. Functional Ecology 11 : 16–23.
Lei TT, Lechowicz MJ. 1997 b. Functional responses of Acer species to
two simulated forest gap environments : leaf-level properties and
photosynthesis. Photosynthetica 33 : 277–289.
Lei TT, Tabuchi R, Kitao M, Koike T. 1996. Functional relationship
between chlorophyll content and leaf reflectance, and light
capturing efficiency of Japanese forest species. Physiologia
Plantarum 96 : 411–418.
Lei TT, Tabuchi R, Kitao M, Takahashi K, Koike T. 1998. Effects of
season, weather and vertical position on the variation in light
quantity and quality in a Japanese deciduous broadleaf forest.
Journal of Sustainable Forestry 6 : 35–55.
Lieberman D, Lieberman M, Peralta R. 1989. Forests are not just swiss
cheese : canopy stereogeometry of non-gaps in tropical forests.
Ecology 70 : 550–552.
Maeglin RR, Ohmann LF. 1973. Boxelder (Acer negundo) : a review and
commentary. Bulletin of the Torrey Botanical Club 100 : 357–363.
Messier C, Bellefleur P. 1988. Light quantity and quality on the forest
floor of pioneer and climax stages in a birch-beech-sugar maple
stand. Canadian Journal of Forest Research 18 : 615–622.
Middleton KR. 1960. New Nessler reagent and its use in the direct
Nesslerization of Kjeldahl digests. Journal of Applied Chemistry
10 : 281–286.
Millard P, Proe MF. 1991. Leaf demography and the seasonal internal
cycling of nitrogen in sycamore (Acer pseudoplatanus L.) seedlings
in relation to nitrogen supply. New Phytologist 117 : 587–596.
Nakashizuka T. 1985. Diffused light conditions in canopy gaps in a
beech (Fagus crenata Blume) forest. Oecologia 66 : 472–474.
Peters R, Tanaka H, Shibata M, Nakashizuka T. 1995. Light climate
and growth in shade-tolerant Fagus crenata, Acer mono and
Carpinus cordata. Ecoscience 2 : 67–74.
Pickett STA, White PS. 1985. The ecology of natural disturbance and
patch dynamics. New York : Academic Press.
Powers HO. 1967. A blade tissue study of forty-seven species and
varieties of Aceraceae. American Midland Naturalist 78 : 301–323.
Riddoch I, Lehto T, Grace J. 1991. Photosynthesis of tropical tree
Lei and Lechowicz—Plasticity of Forest Maples in Simulated Gaps
seedlings in relation to light and nutrient supply. New Phytologist
119 : 137–147.
Runkle JR. 1985. Disturbance regimes in temperate forests. In : Pickett
STA, White PS, eds. The ecology of natural disturbance and patch
dynamics. New York : Academic Press, 17–33.
Runkle JR. 1990. Gap dynamics in an Ohio Acer-Fagus forest and
speculations on the geography of disturbance. Canadian Journal of
Forest Research 20 : 632–641.
SAS Institute Inc. 1989. SAS}STAT user’s guide, Release 6±04 Edition.
Cary, NC.
Sipe TW, Bazzaz FA. 1994. Gap partitioning among maples (Acer) in
central New England : Shoot architecture and photosynthesis.
Ecology 75 : 2318–2332.
Sipe TW, Bazzaz FA. 1995. Gap partitioning among maples (Acer) in
central New England : survival and growth. Ecology 76 : 1587–1602.
St. Jacques C, Bellefleur P. 1993. Light requirements of some broadleaf
tree seedlings in natural conditions. Forest Ecology and Management 56 : 329–341.
Sultan SE. 1992. Phenotypic plasticity and the Neo-Darwinian legacy.
EŠolutionary Trends in Plants 6 : 61–71.
Sultan SE. 1995. Phenotypic plasticity and plant adaptation. Acta
Botanica Neerlandica 44 : 363–383.
Turnbull MH. 1991. The effect of light quantity and quality during
development on the photosynthetic characteristics of six Australian
rainforest tree species. Oecologia 87 : 110–117.
19
Turnbull MH, Yates DJ. 1993. Seasonal variation in the red}far-red
ratio and photon flux density in an Australian sub-tropical
rainforest. Agricultural and Forest Meteorology 64 : 111–127.
Vogelmann HW. 1973. Fog precipitation in the cloud forests of eastern
Mexico. Bioscience 23 : 96–100.
Walters MB, Reich PB. 1996. Are shade tolerance, survival, and
growth linked ? Low light and nitrogen effects on hardwood
seedlings. Ecology 77 : 841–853.
Warrington IJ, Rook DA, Morgan DC, Turnbull HL. 1989. The
influence of simulated shadelight and daylight on growth,
development and photosynthesis of Pinus radiata, Agathis australis
and Dacrydium cupressinum. Plant Cell and EnŠironment 12 :
343–356.
Wayne PM, Bazzaz FA. 1993 a. Morning Šs. afternoon sun patches in
experimental forest gaps : consequences of temporal incongruency
of resources to birch regeneration. Oecologica 94 : 235–243.
Wayne PM, Bazzaz FA. 1993 b. Birch seedling responses to daily time
courses of light in experimental forest gaps and shadehouses.
Ecology 74 : 1500–1515.
Wilson BF, Fischer BC. 1977. Striped maple : shoot growth and bud
formation related to light intensity. Canadian Journal of Forest
Research 7 : 1–7.
Yates DJ. 1989. Shade factors of a range of shade cloth materials. Acta
Horticulturae 257 : 201–217.