全 文 ：Received 30 Jun. 2003 Accepted 22 Sept. 2003
Supported by the Knowlage Innovation Project of The Chinese Academy of Sciences (KSCX1-08), the State Key Basic Research and
Development Plan of China (G1999043507) and the Dutch Royal Academy of Arts and Sciences.
* Author for correspondence.
http://www.chineseplantscience.com
Acta Botanica Sinica
植 物 学 报 2004, 46 (5): 533-541
Responses of Fagus engleriana Seedlings to Light and Nutrient Availability
GUO Ke1,2*, Marinus J. A. WERGER2
(1. Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China;
2. Department of Plant Ecology and Evolutionary Biology, Utrecht University, Utrecht, The Netherlands)
Abstract : The responses of field-grown Fagus engleriana Seem. seedlings to light and soil nutrient
availability were investigated. Two-year-old seedlings were grown for two growing seasons under six
treatment conditions, including three light levels (L1: 1%-2% of full sunlight; L2: 18% of full sunlight; L3:
100% of full sunlight), with and without fertilizer addition (F1 and F0) for each light level. The results showed
that light and nutrients had significant effect on seedling growth as measured in terms of shoot height,
stem basal diameter and biomass; the mean increments of shoot height over two growing seasons were
significantly less in L1 than in L2 and L3 (P ＜0.001), and in L3 than in L2 (P ＜0.01), but the increments
during the first growing season were not significantly different among the treatments; the increments of
stem basal diameter and biomass components were significantly less in L1 than in L2 and L3 (P ＜0.001);
the increments of stem basal diameter and whole plant biomass were not statistically different between L2
and L3; adding fertilizer did not affect the seedling growth under closed forest canopy, but had effect in the
environments with more sunlight. The results suggest that (1) two-year-old F. engleriana seedlings could
survive the conditions of closed forest canopy, but their growth might be severely inhibited; (2 ) the
seedlings could grow as well as or even better in small forest gaps than in open sites; and (3) fertile soil
might enhance seedling growth in forest gaps and open sites, but not under closed forest canopy.
Key words: Fagus engleriana ; light; nutrient; shoot height; biomass; stem basal diameter; relative
growth rates (RGR)
Beech forest is one of the most common forest types in
the temperate regions of North America, Europe, and Japan
(Chabot and Mooney, 1985; Polunin, 1985; Ellenberg, 1988;
Vankat, 1990; Peters, 1997). In those forests beech species
are considered as tolerant to shade or deep-shade condi-
tions (Watt, 1923; Baker, 1950; Loach, 1970; Nakas hizuka
and Numata, 1982b; Hara, 1987; Canham, 1988; 1990;
Ellenberg, 1988; Poulson and Platt, 1989; Grubb et al., 1996;
Peters, 1997). In China, however, beech forests occur only
in the mountains of the subtropical region from 23o to 34o
N, and contain many evergreen tree species and bamboo
species (Wang, 1965; Ts ien et al., 1975; Wu, 1980; Hong
and An, 1993; Zhou and Li, 1994; Ban and Qi, 1995; Cao,
1995; Peters, 1997; Guo, 1999). Occurrence of dense bam-
boo shoots in the understory is considered a limiting factor
in the establis hment of beech t rees (Nakas hizuka and
Numata, 1982a; Hara, 1983; 1985; 1987; Nakashizuka, 1987;
Peters and Ohkubo, 1990; Cao, 1995; Peters, 1997). This
type of forest has been named montane deciduous and
evergreen broad-leaved mixed forests (Wu, 1980), but usu-
ally looks like a deciduous broad-leaved forest in the north-
ern part of its lat itudinal range or in the upper part of its
altitudinal distribution range (Ban and Qi, 1995; Cao, 1995).
In the beech forests of China, especially in the mixed
forests, beech seedlings and saplings are hardly found in
the patches where the canopy is closed or the bamboo
grows vigorously (You, 1962; Tsien et al., 1975; Ban and
Qi, 1995; Cao, 1995; Peters, 1997). Those seedlings occur
infrequently in small gaps and in patches where the canopy
is spars e, or on steep slopes where the canopy is open
(Cao, 1995).
So il nutrient condit ion is an importan t facto r for in-
creased photosynthetic production and improved chance
for survival of seedlings suppressed under shade (Peters,
1997). On the mountain s lopes where the beech forests
occur, soil thickness and nutrients often vary markedly with
topography, inclination and aspects of slopes, concave or
convex slopes, altitude, etc. (Ban and Qi, 1995). Therefore,
in beech forests not only the light, but also nutrien ts are
distributed in patchiness.
The patchy distribution of beech seedlings or saplings
leads to the following hypotheses addressed in this study:
(1) beech seedlings do not tolerate the shade conditions in
the understory of closed forests and they cannot survive
Acta Botanica Sinica 植物学报 Vol.46 No.5 2004534
those conditions for long. For successful regeneration, they
need more favorable light conditions; and (2) soil nutrient
availability affects beech seedling establishment and vig-
orous growth.
We tested these hypotheses in an experiment conducted
in the field during two growing seasons, and evaluated the
responses of Fagus engleriana seedlings in terms of shoot
height, stem basal diameter, biomass components, relative
growth rate, leaf area, and root to shoot ratio.
1 Materials and Methods
1.1 Climate and vegetation of the study site
The experiment was carried out in Daba Forest Farm, a
remote mountain area in northeastern Sichuan, China
(elevation 1 420 m, 32.5o N, 107o E). Mean annual tempera-
ture is 9.6 oC, mean annual p recipitation 1 450 mm, mean
annual potential evaporation 776 mm, and mean annual rela-
tive humidity 83%. The rainy s eason coincides with the
growing seas on, and peaks at 270 mm in June. Growing
season lasts about 170 d from late April to mid-October
(Data from Daba Forest Farm).
The major types of natural vegetat ion from 1 400 m to
2 000 m in altitude are deciduous broad-leaved forests. They
consist of mosaics of patches that are usually dominated
or co-dominated by Fagus eng leriana Seem., F. hayatae
subsp. pashanica, Quercus a liena var. acuteserrata,
Carpinus cordata var. chinensis, and C. fargesiana. Some
patches are co-dominated by any of three birch species
(Betula spp.), which are commonly considered as pioneers
in those fo rests (Zhu, 1983). In the valleys that incis e to
altitudes below 1 400 m some evergreen species, s uch as
Cyclobalanopsis spp. and Lithocarpus spp., are able to
reach the forest canopy.
1.2 Seedlings and their treatments
One thousand two-year-old seedlings of F. engleriana
growing in a tree nursery of the forest farm were trans-
plan ted into 1 000 3.5-L pots containing sandy loam soil
obtained from the local forest at 5-20 cm depth. They were
returned to the nursery (with full sunlight) to acclimate to
the new growth conditions and to let the roots (especially
the fine roots) to recover for a period from autumn to next
spring. One week before bud flush in spring, 30 seedlings
were randomly selected from among 763 healthy seedlings
and harvested to obtain initial values of growth variables.
The remaining seedlings (n = 733) were divided randomly
into six g roups, and moved to the experimental environ-
ments in the beech forest: two groups for each of the three
light levels (see below), with one group receiving fertilizer
treatment.
Three light levels were: L1, shaded by a closed forest
canopy with 1%-2% of full sunlight during growing season,
but 60% of full sunlight when leaves were shed; L2, shaded
by a bamboo screen with 18% of full sunlight year round
and some s mall sun flecks of rather short durat ion due to
the open structure of the screen; L3, exposed to full sun-
light in the forest clearing.
Two fertilization treatments were: F0, without fertilizer;
F1, with fertilier addition as nutrient solution at two-month
intervals. The rate of fertilizer application was 100 kg nitro-
gen (N), 20 kg phosphorus (P) and 85 kg potassium (K) per
hectare per year. Apart from the normal rain, the seedlings
were well watered during the growing seasons.
1.3 Harvests, measurement and calculations
Harvests and measurements were performed in April
(t = 0) and October (t = 1) in the first year, and in October
(t = 2) in the following year. Measurements were made of
shoot height (H, mm), stem basal diameter (Bd, mm), leaf
size s caled by length (Ll, mm) and wid th (Lw, mm) of the
blades, and biomass (mg) of roots, main stem, branches
and leaves (Mr, Ms, Mb and Ml, res pectively) after oven
dry ing for 24 h at 80-90 oC. Leaf areas (LA , mm2) were
calculated from a linear regression in the form of:
LA =-18.3 + 0.664 ´ Ll ´ Lw ( r2 = 0.995, P < 0.001 )
The above regres sion equation was based on length
and width measurements of 110 randomly selected leaves.
At t = 0, shoot heights and stem basal diameters of all
seedlings were measured (n = 763). Thirty seedlings were
randomly selected and harvested. Based on the values of
s hoo t heigh t, s tem basal diameter, roo t mas s and
aboveground mass (Ma, mg) of the 30 seedlings, the fol-
lowing regression equations were established:
Mr = 257 + 1.27 ´ H ´ Bd ( r2 = 0.643, P < 0.001 )
Ma =-279 + 1.37 ´ H ´ Bd ( r2 = 0.821, P < 0.001 )
The initial root mass and aboveground mass of the other
733 seedlings were estimated by these equations.
In each group, ten seedlings were randomly selected at
t = 1 and 20 s eedlings at t = 2 and were harvested and
measured.
Leaf mass ratio (LMR), leaf area ratio (LAR) and root to
shoot ratio (R/S) were calculated by the following formulas:
LMR = Ml / M
LAR =LA/M (mm2/mg)
R/S = Mr/Ma
where M is the whole plant biomass.
Relative growth rates (RGR, growing season-1 ) of shoot,
root, and the whole plant were calculated by the fo rmula
given by Hunt (1978):
RGR = [Ln(M2) - Ln (M1)] / (T2-T1)




GUO Ke et al.: Responses of Fagus engleriana Seedlings to Light and Nutrient Availability 539
3.2 Stem basal diameter growth and biomass production
The growth in stem basal diameter was continuous over
the growing season and was proportional to total biomass
increment, which differed among treatments. Differences
were already statistically significant during the first grow-
ing season: Although the mean increments of biomass in
L1F0 and L1F1 did not differ s tatistically from zero in the
first year, they were highly significantly s maller than the
mean increments of treatment L2 and L3 over one and two
growing seasons. This makes the increments in stem basal
diameter and in total biomass a more effective parameter to
measure g rowth response in these deciduous seedlings
than height growth. All this suggests that the growth of
seedlings beneath the closed forest canopy was inhibited
severely, and the low light in tensity of 2% of full sunlight
at the forest floor must be considered a factor limiting car-
bohydrate production and seedling growth. Nevertheless,
the positive increment o f plant biomas s (even excluding
the leaf mass that is largely shed at the end of each growing
season) over two growing seasons in L1 suggests that the
seed lings are able to grow slowly beneath the clos ed
canopy. Popma and Bongers (1988) in their study on the
seedlings of tropical rain forest species found that leaf area
ratio decreased and unit leaf area rate (assimilation rate)
increased with increase in light intensities. The beech seed-
lings in this experiment exhibited similar responses. Rela-
tively larger leaf areas and leaf area rat ios were the main
factors that enabled the seedlings in L2 to grow as well as
the seedlings in L3.
3.3 Allocation of biomass
It has been known for a long time that growth rates of
various parts of a plant are under mutual control and they
are growing in balance (Kozlowski, 1971; Cannell and Dewar,
1994). The seedlings invested proportionally less dry mass
to roots (lower R/S ratio) and more to leaves (higher LMR)
in L1 than in L2 and L3. In L2 and in L3 fertilized seedlings
allocated relat ively less dry mass to roots than non-fertil-
ized seedlings (Table 2; Fig.5). This demonstrated that the
seedlings under the forest canopy tended to increase their
capacity to cap ture ligh t under low light conditions , and
the non-fertilized seedlings tended to enhance their capac-
ity for nutrient uptake under low nutrient conditions. High
transpiration rates in L3 might be another important factor
that led seedlings to partition more dry mas s to roots: the
seedlings in L3F0 partitioned more than half of their assimi-
lates to roots. These seedlings had to meet their needs for
water and nutrients resulting from their high transpiration
rates and high growth rates at the open site. All these dem-
onstrate that allometry o f the s eedlings in the different
treatments could optimize their potential growth.
3.4 Light and nutrient availability
Many shade-tolerant deciduous tree species reach their
maximum photosynthetic rates or growth at approximately
one-th ird to one-half o f full s unligh t (Loach , 1970;
Kozlowski, 1971; Canham, 1988). For the two-year-old F.
engleriana seedlings, the low light intensity under the for-
est canopy seems to be the limiting factor for their growth.
A moderate light intens ity in small gaps as beneath the
bamboo screen can greatly enhance their growth, and fur-
ther increase in gap size and illumination had little effect on
growth.
Although the fertilized seedlings in the open site and
under bamboo s creen grew significan tly better than the
non-fertilized seedlings in this experiment, and nutrients
have been considered beneficial to improve the growth and
the chance for surv ival of beech seedlings suppress ed
under the forest canopy (Peters, 1997), fertilization in this
experiment did not result in a difference in growth, as mea-
sured in terms of height, biomass and stem basal diameter,
between the two treatments beneath the forest canopy.
3.5 Survival and suppression beneath the forest canopy
Canham (1990) found that Fagus grandifolia suffered
periods of suppression prior to recruitment in to canopy
and the average total length of suppression even ranged
from 45 to 52 years. Poulson and Platt (1989) pointed out
that the juveniles could survive in shade for more than 100
years. Fagus crenata was considered to be able to survive
about 10 years in the understory of mature forests in Japan
(Nakashizuka and Numata, 1982b; Hara, 1987; Nakashizuka,
1987; 1988). Other beech species were also considered to
be able to surv ive a number of years at the fores t floor
(Watt , 1923; Zhu and Yang, 1985; Wen and Cao, 1993;
Peters, 1997). In this experiment abou t 10% of the s eed-
lings under the fo rest canopy died and the top parts of
more seedlings died during the first year, but mos t of the
seedlings survived the conditions. The positive increment
of plant biomass (even excluding the leaf mass that is largely
shed at the end of each growing season) over two growing
seasons in L1 demonst rates that the two-year-old seed-
lings are able to slowly grow beneath the canopy, and sur-
vive under those conditions. This suggests that there are
other reas ons why beech seedlings are rare beneath the
closed canopy. The results of this experiment also showed
that small gaps in the forest strongly improve the regenera-
tion of F. engleriana.
Acknowledgements: GUO Ke thanks Prof. LI Bo-Sheng,
Prof. WANG Xian-Pu, Prof. ZHANG Xin-Shi and Dr. CAO
Kun-Fang for their coordination and valuable suggestions,
Acta Botanica Sinica 植物学报 Vol.46 No.5 2004540
and Mr. YUE Wei-Yuan, ZHOU Jun and many other per-
sons in the Daba Forest Farm for their help in this study.
We are grateful to Dr. Heidrun Huber and Dr. Josef F. Stuefer
for their help in data analysis. Financial support from the
Dutch Royal Academy of Arts and Science and the Chi-
nese Ministry of Personnel are gratefully acknowledged.
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