Plant Ecol
DOI 10.1007/s11258-014-0332-0
The contribution of understory light availability and biotic
neighborhood to seedling survival in secondary versus
old-growth temperate forest
Fei Lin • Liza S. Comita • Xugao Wang •
Xuejiao Bai • Zuoqiang Yuan • Dingliang Xing
Zhanqing Hao
•
Received: 30 November 2013 / Accepted: 1 April 2014
Ó Springer Science+Business Media Dordrecht 2014
Abstract Seedling survival plays an important role
in the maintenance of species diversity and forest
dynamics. Although substantial gains have been made
in understanding the factors driving patterns of
seedling survival in forests, few studies have considered the simultaneous contribution of understory light
availability and the local biotic neighborhood to
seedling survival in temperate forests at different
successional stages. Here, we used generalized linear
mixed models to assess the relative importance of
understory light availability and biotic neighborhood
variables on seedling survival in secondary and oldgrowth temperate forest in north eastern China at two
Communicated by Chris Lusk.
Electronic supplementary material The online version of
this article (doi:10.1007/s11258-014-0332-0) contains supplementary material, which is available to authorized users.
F. Lin X. Wang Z. Yuan D. Xing Z. Hao (&)
State Key Laboratory of Forest and Soil Ecology, Institute
of Applied Ecology, Chinese Academy of Sciences,
Shenyang 110164, China
e-mail: [email protected]
F. Lin D. Xing
University of Chinese Academy of Sciences,
Beijing 100049, China
levels (community and guild). At the community
level, biotic neighborhood effects on seedling survival
were more important than understory light availability
in both forests. In both the old-growth and secondary
forests, conspecific basal area had a negative effect on
seedling survival, consistent with negative conspecific
density dependence. At guild levels, the relative
importance of light and biotic neighborhood on
seedling survival showed considerable variation
among guilds in both forests. Available understory
light tended to have positive effects on seedling
survival for shrub and light-demanding species in the
old-growth forest, but negative effects on survival of
shade-tolerant seedlings in the secondary forest. For
tree species and shade-tolerant species, the best fit
models included neighborhood variables, but that was
not the case for shrubs, light-demanding, or mid
shade-tolerant species. Overall, our results
L. S. Comita
Smithsonian Tropical Research Institute, Box
0843-03092, Balboa, Ancón, Republic of Panama
X. Bai
College of Forestry, Shenyang Agricultural University,
Shenyang 110866, China
L. S. Comita
Department of Evolution, Ecology and Organismal
Biology, The Ohio State University, 318 W. 12th Ave.,
Columbus, OH 43210-1293, USA
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demonstrate that the relative importance of understory
light availability and biotic factors on seedling
survival vary with species life-history strategy and
forest successional stage.
Keywords Canopy openness Density
dependence Shade tolerance Species
coexistence Temperate forests
Introduction
Understanding the mechanisms that maintain species
diversity is a central goal in community ecology
(Chesson 2000; Nakashizuka 2001). A number of
different hypotheses have been proposed to explain
species coexistence in tree communities (reviewed by
Nakashizuka 2001; Wright 2002). One set of hypotheses
focuses on the role of the abiotic environment in
promoting species coexistence. Specifically, resourcebased niche hypotheses propose that species diversity is
a function of heterogeneity in resources or habitats, with
different species specializing on different resources or at
given levels of resource availability. For plants, this
mainly refers to variable light and soil resources (Tilman
1982; Bartels and Chen 2010). The effects of such
environmental heterogeneity on seedling establishment,
growth, and survival have been widely investigated in
the context of species coexistence mechanisms (i.e., the
regeneration niche of Grubb 1977). Many studies have
found that spatio-temporal heterogeneity of understory
light to be a crucial component for tree and shrub
regeneration in forest communities (Lieffers and Stadt
1994; Messier 1996; Lieffers et al. 1999; Webb and
Peart 2000; Montgomery and Chazdon 2001; Rüger
et al. 2009; Mejı́a-Domı́nguez et al. 2012). Even subtle
variation in understory light availability can have an
important influence on seedling and sapling growth and
survival (Clark et al. 1996; Kobe 1999; Nicotra et al.
1999; Svenning 2000; Montgomery and Chazdon 2002;
Poorter and Arets 2003). However, some studies have
cast doubt on the role of light partitioning in fostering
species coexistence (Kunstler et al. 2005; Rüger et al.
2011).
In addition to spatial and temporal variation in
abiotic resources, species coexistence in plant communities may be influenced by specialized natural
enemies, such as herbivores and pathogens. According
to the Janzen-Connell hypothesis (Janzen 1970;
123
Connell 1971), juveniles located near conspecific
trees or at high local conspecific densities will suffer
higher mortality as a result of natural enemy attack,
which limits the relative abundance of any one tree
species, and thereby maintains diversity. Many studies
have examined the effects of local biotic neighborhoods on seedling survival and found support for
negative density dependence (NDD) in both temperate
and tropical forests (Clark and Clark 1985; Webb and
Peart 1999; Packer and Clay 2000; HilleRisLambers
et al. 2002; Queenborough et al. 2007; Chen et al.
2010; Comita et al. 2010; Piao et al. 2013). Resourcebased niche partitioning can result in strong intraspecific competition, which may generate patterns of
NDD; however, experimental studies suggest that
natural enemies, rather than competition, are likely
causing observed negative density-dependent seedling
survival in forests (Paine et al. 2008; Mangan et al.
2010).
Although typically examined separately, it is likely
that both abiotic and biotic factors contribute to
seedling survival and play a role in maintaining
diversity. Furthermore, recent studies have found that
the relative importance of abiotic and biotic factors
can vary with time, plant size, and taxonomic scale
(Comita et al. 2009; Queenborough et al. 2009; Chen
et al. 2010; Wang et al. 2012). In addition, the strength
of biotic interactions may vary with abiotic conditions
(e.g., Comita et al. 2009, Lin et al. 2012). Thus, it is
essential to consider both abiotic and biotic factors
when assessing drivers of seedling mortality.
Species with different life-history strategies often
respond differently to abiotic and biotic factors
(Svenning 2000; Hubbell et al. 2001; Gravel et al.
2010). For example, seedlings of shade-tolerant species tend to have higher survival in the shade, whereas
seedlings of light-demanding species experience high
mortality under low light, but have a strong growth
response to canopy openings (Canham 1989; Gravel
et al. 2010; Wright et al. 2010). Also, seedlings of
shade-tolerant species may be less affected by their
local neighborhoods than seedlings of light-demanding species because they are less sensitive to shading,
and have long-lived leaves that are less susceptible to
pathogen and herbivore attack than shorter-lived
leaves of light-demanding species (Coley et al. 1985;
Hubbell et al. 2001; McCarthy-Neumann and Kobe
2008). In addition, differences among species in
growth form (e.g., tree, shrub) may affect the response
Plant Ecol
of seedlings and saplings to local biotic and abiotic
factors (Hubbell et al. 2001; Bai et al. 2012).
The relative importance of abiotic and biotic factors
for seedling survival and species coexistence likely
also varies with forest age. Differences in forest
structure and canopy species composition among
forests of different successional stages are associated
with differing patterns of understory light availability
and seedling establishment (Denslow and Sandra
2000; Guariguata and Ostertag 2001; Peña-Claros
2003; Burton et al. 2009). Furthermore, NDD might be
more prominent in mature forests compared to early
successional forests (Bruelheide et al. 2011). Thus, it
is likely that the relative importance of light availability versus neighbor densities varies with successional stage.
Here, we examine potential drivers of seedling
survival in two temperate forests that differ in
successional stage: a *300 years old mature forest
and a nearby secondary forest that regenerated
following clear cutting *80 years ago. Our previous
studies have shown striking differences in canopy
species composition between the two forests (Hao
et al. 2008a, b): the mature forest is dominated by an
evergreen species (Pinus koraiensis), while the secondary forest is dominated by deciduous species. As a
result, the secondary forest likely experiences larger
seasonal variation in understory light levels over the
course of the year due to community-wide leaf loss in
the fall and flushing in the spring. Research had shown
that temporal heterogeneity in understory light availability may have a significant effect on seedling
regeneration, growth, and carbon gain (Wayne and
Bazzaz 1993; Constabel and Lieffers 1996; Gendron
et al. 2001), especially in mixed temperate and boreal
forests.
In this study, we assessed the relative importance of
understory light availability and local biotic neighborhood variables for seedling survival, and compared
the roles of these drivers between secondary and oldgrowth temperate forests that have different canopy
structures. Specifically, we sought to answer the
following questions: (1) Is understory light availability
or the biotic neighborhood more important in influencing seedling survival? (2) If understory light
availability influences seedling survival, in which
phase of the growing season does it have the greatest
effect? (3) Can life-history strategy be used to predict
the relative importance of factors driving seedling
survival? (4) Do these relationships differ between
early and late successional stages in temperate forests?
Materials and methods
Study site
The study was carried out in a 25 ha (500 m 9
500 m) old-growth, broad-leaved Korean pine
(P. koraiensis) mixed permanent forest plot and a
nearby 5 ha (250 m 9 200 m) secondary permanent
forest plot in the Changbai Nature Reserve, northeastern China. Two pioneer species, poplar (Populus
davidiana) and birch (Betula platyphylla), dominate in
the secondary forest, but the analyses of size-class
distributions indicate that these species will eventually
be replaced by mature forest species, such as P.
koraiensis and Tilla amurensis (Li et al. 2010). The
reserve, established in 1960 along the border of China
and North Korea (127°420 –128°170 E, 41°430 –
42°360 N), is one of the largest biosphere reserves in
China and has been spared from logging and other
severe human disturbances since its establishment in
1960 (Yang and Li 1985). The area has a typical
temperate continental monsoon climate with long,
cold winters and short, and warm summers. Between
1982 and 2003, mean annual precipitation was
695.3 mm, and mean annual temperate was *3.6 °C
with a January (the coldest month) mean of -15.6 °C
and a July (the hottest month) mean of 19.7 °C (Zhang
et al. 2005).
The 25 ha old-growth forest plot was established in
2004 in the most common vegetation type in the
region. The common tree species are P. koraiensis, T.
amurensis, Quercus mongolica, Fraxinus mandshurica, Ulmus japonica, and Acer mono (Hao et al. 2008a).
The 5 ha secondary forest plot was established in
2005, approximately 10 km from the old-growth
forest plot, and contains forest that regenerated
naturally after clear cutting in the 1930s. The secondary poplar-birch forest is an early successional stage of
the broad-leaved Korean pine mixed forest (Hao et al.
2008b).
Within the two plots, all individuals C1 cm diameter at breast height (1.3 m above ground; dbh) were
mapped, tagged, measured, and identified to species
following a standard field protocol (Condit 1998). The
second censuses were carried out in 2009 and 2010 for
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the old-growth and secondary forest plots, respectively. Detailed descriptions of the two sites are
provided in Table S1 (also see Wang et al. 2011;
Zhang et al. 2013).
heterospecific adults within 10 m of the focal seedling,
divided by the distance of each adult from the focal
seedling (Canham et al. 2004; Comita and Hubbell
2009):
Seedling census
A¼
N
X
BAi =DISTANCEi ;
i
We established 600 5 9 5 m seedling plots in 2006 in
the 25 ha old-growth forest plot, and 120 5 9 5 m
seedling plots in 2010 in the 5 ha secondary forest plot
(see detailed descriptions in Bai et al. 2012). At each
seedling plot, all tree seedlings with DBH \ 1 cm,
and shrub and liana seedlings with height B30 cm
were mapped, tagged, measured, and identified to
species. All seedling plots were recensused annually in
August and September. Here, we used seedling data
from 2010 to 2011.
Understory light availability
We characterized understory light availability by
measuring canopy openness above 246 seedling plots
in the old-growth forest site and 43 seedling plots in
the secondary forest site (Fig. S1). The distance
between any two focal seedling plots was at least 8 m.
We took hemispherical photographs at each chosen
seedling plot in three seasons (spring, summer, and
autumn) in 2010. We took photographs on May 12–18
during bud burst, on August 19–22 during full leafing,
and on October 24–26 with leaves off. Hemispherical
photographs were taken in a fixed corner of each
seedling plot at a height of 1 m using a Nikon Coolpix
5000 camera with a FC-E8 fisheye lens. The camera
was horizontally mounted on a tripod, and the top of
photographs was fixed to magnetic north (Montes et al.
2008). We chose homogeneous sky conditions to take
photographs and used Gap Light Analyzer software
(GLA, version 2.0) to analyze the photos and estimate
canopy openness (Frazer et al. 1999). All photographs
were analyzed by the same person to minimize
variation in threshold selection (Valladares and Guzmán 2006.
Biotic factors
For each seedling, we summed the number of
conspecific and heterospecific seedling neighbors
within the seedling plot. We also calculated the sum
of the basal area (BA) of conspecific and
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where i is an individual adult. To eliminate edge
effects, we only included seedlings located [10 m
from the plot boundary.
Data analysis
Because canopy openness values were not normally
distributed with equal variance, we used Wilcoxon
rank sum tests (equivalent to Mann–Whitney tests) to
test for the differences in canopy openness between
the old-growth and the secondary forest sites in each
season.
Because of the height at which hemispherical
photographs were taken, only seedlings B1 m tall in
2010 were considered as focal seedlings in our
analysis. A total of 7017 (tree 77.3 %; shrub 22.7 %)
and 878 (tree 60.6 %; shrub 39.4 %) focal seedlings
were monitored in the old-growth and secondary forest
sites, respectively. We modeled the probability of
individual seedling survival from 2010 to 2011 as a
function of canopy openness and biotic neighborhood
variables, using generalized linear mixed-effects
models (GLMM; Zurr et al. 2009) with binomial
errors. Biotic neighborhood variables included conspecific and heterospecific seedling density, and basal
area of conspecific and heterospecific adult neighbors
within 10 m of focal seedlings, as described above. All
variables, as well as log-transformed initial seedling
height, entered the model as fixed effects. For
comparing the relative importance of variables and
the difference between two forest types directly, the
values of all continuous explanatory variables were
standardized by subtracting the mean value of the
variable (across all individuals of the two sites in the
analysis) and dividing by 1 standard deviation (Gelman and Hill 2006). The mean and range of biotic
variables used in the analysis are listed in Table S2. In
all models, seedling plot was included as a random
effect to account for spatial autocorrelation in mortality of seedlings located within the same plot. In
addition, species was included as a random effect to
Results
Seasonal variation in canopy openness
Canopy openness varied significantly during the
growing season and was larger in the spring and
autumn than in the summer in both sites (Fig. 1). In the
spring, canopy openness in the secondary site was
significantly lower than in the old-growth site
(W = 7,138, p = 0.007), but was significantly higher
in the autumn (W = 24, p \ 0.001). In the summer,
canopy openness did not differ significantly between
the two sites (W = 6,655.5, p = 0.07).
Community-level analysis of seedling survival
Over the study period, 36.4 % of seedlings survived in
the old-growth forest site and 81.6 % of seedlings
40
30
20
10
Canopy openness (%)
50
Old-growth forest
Secondary forest
0
account for variation among species in baseline
survival rates.
To test the relative importance of available understory light and biotic variables for seedling survival in
old-growth and secondary forests, four candidate
models were constructed: (1) a null model with only
seedling height and random effects; (2) a light model
in which canopy openness was added to the null
model; (3) a biotic model in which biotic variables
were added to the null model; (4) a full model
including all variables (seedling height, canopy openness, and biotic variables). For models including
canopy openness (models 2 and 4), we ran the models
separately for each of the three seasons in which
canopy openness was measured. We compared models
using Akaike’s Information Criterion (AIC: Burnham
and Anderson 2002). The model with the smallest AIC
value was considered the best fit model, although
models within 2 units are generally considered to have
equal weight.
Seedling survival was analyzed at two different
levels in the two sites separately: (1) the community
level with all seedlings combined, (2) the guild level,
with growth forms (tree and shrub) and shade tolerance guilds (light-demanding, mid shade-tolerant, and
shade-tolerant, from Wang et al. 2009) each analyzed
separately. All analyses were carried out in R Software
(Version 2.15.1; R Core Team, 2012), using the
‘‘lme4’’ package (Bates et al. 2012).
60
Plant Ecol
Spring
Summer
Autumn
Fig. 1 Changes in canopy openness with season. Boxplots
show median (line), 25th and 75th percentiles (box), the location
of the most extreme data points within 1.5 times the length of the
box (whiskers) and singular values beyond the whiskers (circles)
for canopy openness in the old-growth and secondary forest sites
survived in the secondary forest site (Table S3). At the
Community level, the biotic model, which included
conspecific and heterospecific neighbor densities, was
the best fit model for seedling survival in both sites,
but could not be statistically differentiated from the
full models, which also included light availability (i.e.,
the difference in AIC \ 2; Table 1).
Seedling height showed the strongest positive
effect on seedling survival in both sites (Fig. 2). The
basal area of conspecific neighbors had a significant
negative effect in the old-growth site and a marginally
significant negative effect in the secondary site
(p = 0.052; Figs. 2, 5). There were no significant
effects of conspecific seedling density, heterospecific
seedling density or heterospecific basal area. In
addition, effects of canopy openness on seedling
survival were not significant in any season in either the
light or full models for either site.
Guild level analysis
Growth form: trees versus shrubs
For tree species, the biotic model was the best fit
model in both sites, but models that contained canopy
openness, as well as the null model, were within 2 AIC
units (Table 1). Of the individual variables included in
the best fit model, only seedling height had a
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Table 1 AIC values of the generalized linear mixed models of seedling survival at the community and guild level in the old-growth
and secondary forest sites
Candidate model
Season
All species
Growth form
Tree
Shade tolerance
Shrub
Light-demanding
Mid shade-tolerant
Shade-tolerant
Old-growth site
Null (height)
5,046.287
3,930.699
1,052.782
155.7397
1,675.119
2,610.59
Biotic
5,041.015
3,929.248
1,059.227
159.9171
1,679.182
2,604.952
Light
Biotic ? light
Spring
5,047.172
3,931.733
1,054.596
154.7508
1,676.883
2,609.885
Summer
5,048.277
3,932.28
1,050.193
157.4647
1,676.885
2,612.453
Autumn
5,047.956
3,931.714
1,054.203
152.1882
1,675.653
2,611.778
Spring
5,042.372
3,930.723
1,061.068
158.9842
1,681.148
2,604.738
Summer
5,042.976
3,931.109
1,057.447
161.0302
1,681.158
2,606.946
Autumn
5,042.865
3,930.614
1,060.692
154.836
1,679.922
2,606.361
Secondary site
Null (height)
Biotic
Light
Biotic ? light
698.621
694.0393
487.7499
487.3347
215.3485
217.9881
146.0819
151.1586
274.2406
278.9155
243.7506
240.9462
Spring
700.604
489.7463
216.9443
147.8994
276.0438
243.6887
Summer
700.4588
489.633
217.1796
147.4277
275.7566
245.609
Autumn
699.4811
489.2819
216.0741
148.077
276.1431
244.8243
Spring
696.0121
489.3234
219.8636
152.776
280.8557
242.9124
Summer
696.0129
489.2934
219.4152
152.8577
280.8421
242.3297
Autumn
694.9316
488.8428
218.2902
153.1562
280.8961
238.3934
The most likely models are shown in bold
significant effect on tree seedling survival (Fig. 3). For
shrubs, the light model that included canopy openness
in the summer was the best fit in the old-growth site
(Table 1). Both seedling height and canopy openness
had significant positive effects on shrub survival
(Figs. 3, 5). In the second-growth site, the null model
was the best fit model, but all of the light models were
within 2 AIC units (Table 1). However, none of the
individual variables (i.e., seedling height, canopy
openness in different seasons) were significant
(Fig. 3).
Old-growth forest
Intercept
Secondary forest
Model parameters
ln Height
Conspecific
seedling
density
Heterospecific
seedling
density
Conspecific
basal area
Shade tolerance guilds
Heterospecific
basal area
-5
-4
-3
-2
-1
0
1
2
Coefficient estimate
Fig. 2 Estimated effects (±2 SE) of variables on seedling
survival at the Community level for the most likely models (see
Table 1) in the old-growth and secondary forest sites. Models
were run separately for each forest site (circles old-growth,
triangles secondary), but parameter values are presented on a
single graph to facilitate comparison. Filled symbols indicate
significant effects (p \ 0.05)
123
Results varied among the three shade tolerance guilds.
For the light-demanding group, the light model in the
autumn was the best fit model in the old-growth site,
and both seedling height and canopy openness had
significant positive effects on seedling survival
(Table 1; Figs. 4, 5). However in the secondary site,
the null model was the most likely model, although the
light models were all within 2 AIC units (Table 1).
There were no significant effects of seedling height or
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B
A
C
D
ln Height
Canopy
openness
Model parameters
Fig. 3 Estimated effects
(±2 SE) of variables on
seedling survival for the
most likely model for each
growth form (trees, shrubs).
a trees in the old-growth
forest site; b trees in the
secondary forest site;
c shrubs in the old-growth
forest site; d shrubs in the
secondary forest site. Filled
symbols indicate significant
effects (p \ 0.05). Note
difference in x-axis ranges
Conspecific
seedling
density
Heterospecific
seedling
density
Conspecific
basal area
Heterospecific
basal area
-1
1
2
3
-5
-2
0
2
-1
0
1
2
-1
1
3
Coefficient estimate
canopy openness in any season for light-demanding
species in the secondary forest (Fig. 4). For the mid
shade-tolerant group, the null model was the best fit
model in both sites, with seedling height having a
significant positive effect on seedling survival. For
both sites, the light models were all within 2 AIC units
(Table 1), but effects on canopy openness on survival
were not significant. For the shade-tolerant group, the
full model with canopy openness in the spring was the
best fit model in the old-growth site, but could not be
statistically differentiated from the biotic model and
the full model with canopy openness in the autumn
(i.e., AIC within 2 units). For the best fit model,
seedling height had a significant positive effect on
survival and conspecific seedling density and basal
area of conspecific adult neighbors had marginally
significant positive and negative effects, respectively
(p = 0.055 and 0.068, respectively) (Fig. 4). For
shade-tolerant species in the secondary forest site,
the full model with canopy openness in the autumn
was the best fit model. Canopy openness and heterospecific seedling density both had significant negative effects on survival, while seedling height had a
significant positive effect. Basal area of conspecific
adult neighbors had a marginally significant negative
effect (p = 0.056); Figs. 4, 5).
Discussion
Variation in understory light availability
with season and forest type
Our results clearly demonstrated seasonal variation of
light availability (i.e., canopy openness) in both
forests, but differences in canopy openness between
the two forests changed with season. Seasonal variation of canopy openness within and between forests
was mainly influenced by phenology, tree species
composition, and stand age (Smith 1982; Brown and
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Plant Ecol
understory light availability and result in changing
patterns with successional stage, particularly in temperate and boreal forests.
Parker 1994; Messier et al. 1998). In the spring, the
old-growth forest tended to have larger canopy
openness values than the secondary forest. One
possible reason is that the trees in the secondary forest
put out leaves earlier or faster than those in the oldgrowth forest. In the summer, trees in both forests are
in full leaf, which resulted in similar values of canopy
openness. In the autumn, however, the old-growth
forest had lower canopy openness than the secondary
forest likely because of the higher abundance of
evergreen adult coniferous trees (mainly Korean pine)
in the old-growth forest than in the secondary forest.
These results are similar to patterns of seasonal
variation in understory light availability reported for
a boreal forest in North America, where differences
between younger and older forests were also due to
differences in the abundance of evergreen species
(Constabel and Lieffers 1996). Together with our
results, this highlights how species composition,
particularly the abundance of deciduous versus evergreen species, can influence temporal variation in
A
Relative importance of understory light
availability and biotic factors for seedling survival
At the community level, we found that the biotic
neighborhood had a stronger impact on seedling
survival than understory light availability in both the
old-growth and secondary forests. In particular, we
found a significant negative effect of conspecific adult
neighbors on seedling survival, consistent with the
Janzen-Connell hypothesis (Janzen 1970; Connell
1971). This hypothesis was originally proposed to
explain the maintenance of diversity in tropical
forests. However, our results, along with other recent
studies (e.g., HilleRisLambers et al. 2002, Bai et al.
2012, Johnson et al. 2012), suggest that conspecific
negative density dependence also plays a role in
structuring temperate forests.
B
C
D
E
F
1
3 -10 -4
ln Height
Model parameters
Canopy
openness
Conspecific
seedling
density
Heterospecific
seedling
density
Conspecific
basal area
Heterospecific
basal area
-1 1 3 5
-2
0
2
-1
1
3
-1
1
3
-1
1
Coefficient estimate
Fig. 4 Estimated effects (±2 SE) of variables on seedling
survival for the most likely model for each shade tolerance guild
(light-demanding, mid shade-tolerant, shade-tolerant). a lightdemanding guild in the old-growth forest site; b light-demanding guild in the secondary forest site; c mid shade-tolerant guild
123
in the old-growth forest site; d mid shade-tolerant guild in the
secondary forest site. e shade-tolerant guild in the old-growth
forest site; f shade-tolerant guild in the secondary forest site.
Filled symbols indicate significant effects (p \ 0.05). Note
differences in x-axis ranges
Plant Ecol
C
D
E
0.6
1.2
0.8
0.6
0.80
11
14
0.4
0.55
0.84
0.0
Conspecific basal
area
0.90
0.75
0.65
0.88
0.15
0.92
0.25
0.85
B
0.05
Probability of survival
A
26
17
Canopy openness
(%)
30
34
Canopy openness
(%)
35
45
55
10
40
70
Canopy openness Heterospecific seedling
(%)
neighbors
Fig. 5 The strength of the effects of variables (except seedling
height) that had significant impacts on the probability of survival
for seedlings based on parameter values from the best fit models
at the community level and for specific guilds. a effect of
conspecific neighbors, defined as the summed distanceweighted basal area of conspecific trees C1 cm DBH within
10 m of the seedling plot, at the community level in the oldgrowth forest site. b effect of canopy openness on shrubs in the
old-growth forest site. c effect of canopy openness on the lightdemanding guild in the old-growth forest site. d effect of canopy
openness on the shade-tolerant guild in the secondary forest site.
e effect of heterospecific seedling neighbors, calculated as the
number of heterospecific seedlings occurring within the same
5 9 5 m quadrat as the focal seedling, on the shade-tolerant
guild in the secondary forest site
Although many studies have demonstrated that
understory light availability has significant effects on
seedling survival in temperate forests (e.g., Osunkjoya
et al. 1992; Kobe 1999; Beckage and Clark 2003), we
found that understory light availability did not have a
significant effect on seedling survival at the community level at our sites. Rather, the impacts of understory light availability appear to vary among species
that differ in ecological strategy. Specifically, we
found significant effects of light availability when
examining ecological guilds separately (discussed
below), suggesting that light does play a role in
structuring the temperate forest communities studied
here.
negative density dependence as forest succession
proceeds (Chazdon 2008).
While the seedling community in both forests
showed similar responses to abiotic and biotic variables, seedling survival was substantially higher in the
secondary forest than in the old-growth forest (81 vs.
36 %, respectively). This may be due in part to a
higher abundance of deciduous trees, which allows
more light to reach the forest floor over the course of
the year (Osunkjoya et al. 1992). Thus, while spatial
variation in light availability may not impact seedling
survival within each forest, the large difference in light
availability between forests, particularly in the
autumn, may explain differences in seedling survival
between the two forests. Differences in survival
between the two forests could also reflect differences
in the biotic neighborhoods. Specifically, the maximum conspecific neighbor densities encountered were
much larger in the old-growth than the secondary
forest (Table S2), which would lead to lower seedling
survival based on our model results.
Differences in drivers of seedling survival in oldgrowth versus secondary forest
At the community level, we found little difference
between the old-growth and secondary forest in terms
of the dominant drivers of seedling survival. In both
forests, the biotic model was the best fit model, and no
significant effects of light availability on communitywide seedling survival were detected. In both forests,
we found a negative effect of conspecific basal area on
seedling survival, although this effect was only
marginally significant in the secondary forest. This
may reflect a trend of increasing importance of
Variation among ecological guilds
We found considerable differences among ecological
guilds in the factors driving seedling survival. Tree
seedlings in both forests were predominantly impacted
by the biotic neighborhood, while shrub seedlings
123
Plant Ecol
were more strongly impacted by understory light
availability than biotic neighborhood variables in the
old-growth forest. This is consistent with the study of
Bai et al. (2012), which similarly found that biotic
factors had no effect on shrub seedling survival.
Instead, they found limited support for a role of
topographic and edaphic factors in driving shrub
seedling survival in the Changbaishan old-growth
forest. Our study demonstrated that canopy openness
also influences shrub seedling survival. However, in
the secondary forest, seedling survival of shrubs was
not significantly affected by understory light. This
may be because the higher overall canopy openness in
the secondary forest creates a favorable environment
for shrubs throughout the site, reflected by the very
high survival of shrub seedlings in the secondary
forest site (91 %; Table S3).
When examining the shade tolerance guilds separately, we found that available understory light was a
crucial habitat factor in both forests. As expected,
survival of light-demanding species in the old-growth
forest was positively influenced by understory light
availability. Interestingly, we found that canopy
openness in the spring and summer did not significantly affect survival of light-demanding seedlings;
only autumn canopy openness had an effect. This
suggests that light-demanding seedlings growing
beneath trees of deciduous species that lose their
leaves in the autumn had better survival than those
growing beneath evergreen species that retained their
leaves. This would also explain why we failed to
detect significant effects of canopy openness on
survival of light-demanding seedlings in the secondary
forest, which is dominated by deciduous species, and
therefore, would have high canopy openness throughout the site in the autumn. These results support the
idea that some understory plants can survive through
additional photosynthetic production at high light
levels in the autumn due to leaf loss of canopy trees,
and that these characteristics tend to be more acute in
old-growth forests than in earlier successional forests
(Messier et al. 2009).
In contrast to light-demanding species, shadetolerant species tended to show reduced seedling
survival at higher understory light levels. This was
particularly true in the secondary forest site in the
autumn, when canopy openness was highest, again
highlighting the importance of light availability at
the end of growing season. This result is contrary to
123
results from a number of studies that have found
higher light levels usually enhance seedling survival,
even for shade-tolerant species (e.g., Kobe et al.
1995; Lusk and Del Pozo 2002; Montgomery and
Chazdon 2002). However, very high light levels
have been found to result in decreased seedling
survival (e.g., Comita et al. 2009). Shade-tolerant
seedlings in particular may be negatively impacted
under high-light conditions due to strong competition from light-demanding species or to photoinhibition (Krause et al. 2001).
Seedling survival of shade-tolerant species was also
influenced by the biotic neighborhood. In the oldgrowth forest, the density of conspecific seedling
neighbors showed a marginally significant positive
effect on survival. This effect is likely due to a habitat
effect, rather than facilitation: for species with habitat
preferences, recruitment will be high at sites with
conditions that promote survival of that species,
resulting in high conspecific seedling densities. If
conditions remain beneficial for survival, those high
density sites will have high survival, resulting in a
positive correlation between conspecific density and
survival. If effects of habitat preference on seedling
survival were greater than those of density-dependent
natural enemies, survival could have a positive
relation with conspecific seedling density, potentially
masking negative impacts of conspecific neighbors
(Comita and Hubbell 2009). In the secondary forest,
among biotic factors, only heterospecific seedling
neighbors had a significant effect on seedling survival
for shade-tolerant species, with survival negatively
impacted by heterospecific seedling density. This
likely reflects the fact that shade-tolerant seedlings are
weaker competitors than light-demanding seedlings in
high light environments (Walters and Reich 1996;
Valladares and Niinemets 2008).
Limitations
The present work has some limitations. First, sample size
in our analysis is relatively limited, which may influence
the possibility to detect significant effects of factors,
particularly in the secondary forest. Second, only one oldgrowth forest and one secondary forest were included,
limiting the generalizations that can be drawn. Third, we
only examined drivers of survival over a single year. It is
possible that the main drivers of seedling survival vary
over time, with periodic events such as mast seeding or
Plant Ecol
severe storms having strong impacts on seedling dynamics in some years. Thus, long-term data are needed on
seedling dynamics. Finally, other factors, such as soil pH,
nutrient availability, water availability and pathogen, and
insect attack, which may affect seedling survival were not
explicitly included in the analysis.
Conclusion
Few studies have explored the response of seedling
survival to understory light availability and local
biotic neighborhood variables simultaneously within
forests of different successional stages, even though
this information is necessary to understand successional dynamics. In our study, although there was
significant variation in canopy openness, we found
that understory light availability did not explain
seedling survival at the community level in either
site. Rather, the biotic neighborhood played a relatively more important role in driving seedling survival
at the community level, with negative impacts of
conspecific neighbors on seedling survival, consistent
with negative density dependence. However, the
relative importance of understory light availability
varied dramatically among guilds, with different guild
level effects in the old-growth and secondary forest
sites. Overall, our results suggest that variation in
species life-history traits, along with negative density
dependence, could contribute to coexistence and drive
patterns of succession in temperate forests.
Acknowledgments This work was supported by the National
Natural Science and Foundation of China (41101188,
31370444, and 41301057) and State Key Laboratory of Forest
and Soil Ecology (LFSE2013-11). We thank Dr. Jiaojun Zhu for
his valuable suggestions for methods. We thank Dr. Simon
Queenborough for assistance with the figures. We also thank
Liwei Wang, Ji Ye, Buhang Li, Zhaochen Zhang, Xu Kuang,
Houjuan Song, Guodong Liu, Baizhang Song and Zhenshan Li
for their assistance with the data collection.
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