Forest Ecology and Management 479 (2021) 118540

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Forest Ecology and Management

journal homepage: www.elsevier.com/locate/foreco

Scale-dependent changes in the contributions of biotic and abiotic factors to T

leaf area index in a natural forest in northeast China
Zhili Liua,b, Bin Lia, Guangze Jina,b,
⁎

a
Center for Ecological Research, Northeast Forestry University, Harbin 150040, China
b
Key Laboratory of Sustainable Forest Ecosystem Management-Ministry of Education, Northeast Forestry University, Harbin 150040, China

ARTICLE INFO ABSTRACT

Keywords: The leaf area index (LAI) is one of the most commonly used parameters for quantifying canopy structure and
Structural equation modeling (SEM) predicting vegetation growth. However, it remains unclear whether the relative contributions of biotic factors
Leaf area index (LAI) and abiotic factors to stand LAI are modulated by the study scale (or plot size). Additionally, whether tree size
Plot size affects the contributions of biotic factors to the LAI is unknown. In this study, we measured LAI with a LAI-2200
Tree size
plant canopy analyzer in subplots of three scales (i.e., 10 m × 10 m, 20 m × 20 m and 30 m × 30 m) in a 9 ha
Basal area
Stand density
old-growth forest plot in northeast China. We also measured biotic factors for large trees (diameter at breast
Species richness height, DBH > 9 cm) and small trees (DBH ≤ 9 cm) as well as abiotic factors (e.g., soil properties and light
availability quantified by hillshade) in each subplot for three scales. With structural equation modeling (SEM),
we found that an increase in the basal area of large trees directly reduced the stand LAI at all three scales and
indirectly reduced the LAI by limiting the growth of small trees, but increased stand density (or basal area) for
small trees increased the stand LAI. The increased species richness of small trees enhanced the LAI at
10 m × 10 m and 20 m × 20 m; in contrast, the increased species richness of large trees only significantly
reduced the LAI at 20 m × 20 m. Increases in a soil property (total phosphorus) directly reduced the LAI at all
three scales, but increased light increased the LAI. We also found that the contribution of large trees to LAI was
higher at smaller scales but that of small trees increased with increasing scale; the contribution of soil properties
to the LAI increased with increasing scale, but light made higher contributions at smaller scales. These results
clearly suggest that the relative contributions of biotic factors and abiotic factors to stand LAI are scale-de-
pendent and that tree size plays a key role in revealing the relationships between biotic factors and stand LAI in
natural forests.

1. Introduction
The leaf area index (LAI) quantifies the amount of leaf area per unit
of horizontal ground surface area (Chen & Black, 1992). It is an es-
sential factor in modeling plant dynamic changes, photosynthesis, and
carbon or water cycles between forest canopies and the atmosphere
(Capdevielle-Vargas et al., 2015; Wu et al., 2016; Toda & Richardson,
2018; Chen et al., 2019). The variations in LAI in forest ecosystems
limit efforts to model these ecological processes at multiple spatial
scales (Spadavecchia et al., 2008; Richardson et al., 2013; Fang et al.,
2019). Therefore, revealing the cause of LAI variation is a consistently
important issue (Bequet et al., 2012a; Öztürk et al., 2015; Yan et al.,
2016; Zhu et al., 2016; Niinemets & Tobias, 2019).
Biotic factors, such as stand structure (e.g., density, basal area or
diameter at breast height, DBH), species diversity and tree size
distribution, are major driving factors of the forest canopy structure
(Medhurst & Beadle, 2001; Bequet et al., 2012a; Zhang & Chen, 2015;
Ali et al., 2019b) and thus the LAI. A series of studies have shown that
biotic factors have the potential to promote LAI. For example, planta-
tions with a high basal area or stand density generally have higher LAI
(Bequet et al., 2012b; Fotis et al., 2018). However, in natural forests,
plants vary in size, leading to a multilayered stand structure and thus
enhancing light capture and increasing light-resource-use efficiency
within a site (Yachi & Loreau, 2007; Bartels & Chen, 2010). Recent
studies indicate that tree size inequality is linked with stand structure
diversity and hence aboveground biomass variation (Zhang & Chen,
2015; Ali et al., 2019b). For example, a large portion of the above-
ground biomass and basal area was contributed by a few large trees
relative to the proportion contributed by other trees in natural forests
(Xu et al., 2015; Bastin et al., 2018; Lutz et al., 2018; Ali et al., 2019b).

⁎
Corresponding author.
E-mail address: taxus@126.com (G. Jin).

https://doi.org/10.1016/j.foreco.2020.118540
Received 28 July 2020; Received in revised form 25 August 2020; Accepted 27 August 2020
Available online 06 September 2020
0378-1127/ © 2020 Elsevier B.V. All rights reserved.
Z. Liu, et al.
Stand structurelarge
Soil properties
Stand structuresmall
LAI
Fig. 1. Conceptual framework linking biotic factors (stand structure and species richness for large trees and small trees) and abiotic factors (soil properties and
hillshade) to the LAI.
However, leaf biomass only comprises a small part (usually less than
5%) of aboveground biomass (Wang, 2006; Cai et al., 2016), and the
large trees usually have greater canopy area than small trees; thus, the
contribution of large trees to the stand LAI may not necessarily be
greater than that of small trees. In addition, large trees with high basal
area, which can be used as a proxy for high competition intensity, will
limit the amount of light, soil nutrients and water available to small
trees (Paquette & Messier, 2010; Slik et al., 2013; Ali et al., 2019a). This
reduces the density and species richness of small trees, thus reducing
the stand LAI. Therefore, a high basal area that is mainly determined by
a few large trees may not lead to higher stand LAI in a natural forest. In
contrast, a high basal area or high density of small trees is likely to
enhance stand LAI.
Not only biotic factors (e.g., density and basal area) but also abiotic
factors (e.g., soil nutrients and light) are important drivers of LAI.
Previous studies have shown that abundant light, soil nutrients and soil
water are conducive to plant growth (Meinzer et al., 2011; van der
Sande et al., 2017; Yuan et al., 2019) and therefore may increase LAI,
mainly because these resources are usually the limiting factors for plant
growth. Moreover, these abiotic factors can also indirectly determine
LAI changes by regulating biotic factors. In a natural forest, forest
vertical stratification is very complicated and directly affects the soil
available resources and light interception (Cavaleri et al., 2010;
Meinzer et al., 2011). For example, soil nutrients are more plentiful for
large trees because of the dominant filtering role of large trees on the
available resources, which limits resource availability for small trees
(Quesada et al., 2012). Similarly, the amount of light is generally suf-
ficient for overstory trees (i.e., large trees), while it is the most limiting
resource for understory trees (i.e., small trees) (Meinzer et al., 2011;
Tinya & Ódor, 2016; Liu et al., 2020). In this case, abundant light will
enhance the density or species richness of small trees and thus increase
stand LAI, but it may have less influence on those of large trees.
In addition, topographic variables are reported to affect plant
growth and LAI mainly because these factors usually determine the
distribution of light and soil conditions (Spadavecchia et al., 2008; Lan
et al., 2011). The increased elevation is linked with lower temperature
and higher insolation (Li et al., 2006; Spadavecchia et al., 2008), and
the greater the slope is, the lower the soil moisture. Moreover, the re-
lationships between topographic variables and LAI may vary with scale
(Spadavecchia et al., 2008). These findings suggest that the LAI in a
natural forest is determined in a complex process; the LAI may be in-
fluenced by various factors, and some factors may indirectly affect the
LAI by modifying other factors.
Scale or plot size should also be considered in estimating LAI
(Garrigues et al., 2006; Spadavecchia et al., 2008; Xu et al., 2009; Yan
et al., 2016). To maximize the use of resources, two large trees in a
2
Forest Ecology and Management 479 (2021) 118540
Species richnesslarge
Hillshade
Species richnesssmall
natural forest will not be too close to each other to avoid competition
(Bequet et al., 2012b), which results in the pattern of a few small shade-
tolerant trees surrounding a large tree. However, for trees beyond the
control of resources by large trees, there are more abundant resources
(e.g., light, soil nutrients) and less competition to support the survival
and growth of more individuals (Sambakhe et al., 2014). Therefore, if
the plot size for estimating LAI is relatively small and within the control
range of a large tree, the contributions of the large tree to LAI variations
are likely to be greater than those of the small trees. As the plot size
increases, more small trees become involved; the contributions of the
large tree decrease, and those of the small tree increase. In this case, the
contribution of the small trees to LAI variations may be greater than
that of the large tree. However, this situation has never been examined
in a natural forest.
In the present study, we use a uniquely detailed data set on LAI,
stand structure (basal area, density and DBH) and species richness
across the forest strata (i.e., large trees and small trees), soil properties
(soil nutrients and soil water availability) and topography (hillshade for
characterizing light availability) in a large permanent old-growth
temperate forest to investigate the biotic and abiotic drivers that shape
LAI variation. The data were collected at three resolutions, i.e.,
10 m × 10 m, 20 m × 20 m and 30 m × 30 m. We developed a
conceptual model for LAI in which biotic factors and abiotic factors may
have direct and indirect effects through the modification of other fac-
tors (Fig. 1). We used structural equation modeling (SEM) to analyze
the LAI based on the conceptual model at the three scales. We address
the following questions. 1) How do biotic factors drive LAI variations?
We hypothesize that both the stand structure and species richness of
large trees are negatively correlated with LAI but that those of small
trees are positively correlated with LAI. The stand structure of large
trees limits the stand structure and species richness of small trees, but
the species richness of large trees enhances the stand structure and
species richness of small trees. 2) How do abiotic factors drive LAI
variation? We hypothesize that soil properties and light not only have
strong direct effects on the LAI but also indirectly affect the LAI by
regulating biotic factors and that these effects could differ and even
show opposite trends between large trees and small trees. 3) How does
plot size change the contributions of biotic factors and abiotic factors to
LAI variations? We hypothesize that the contributions of large trees to
LAI variation decrease and those of small trees increase with increasing
plot size and that the contributions of large trees are higher than those
of small trees at smaller plot sizes, with the opposite result at larger plot
sizes.
Z. Liu, et al. Forest Ecology and Management 479 (2021) 118540

Fig. 2. Structural equation models of the effects of

(a) 10 m × 10 m
Basal arealarge Species richnesslarge biotic factors (stand structure and species richness for
-0.341*** large trees and small trees) and abiotic factors (soil
properties and hillshade) on the LAI at three sam-
pling scales: (a) 10 m × 10 m, (b) 20 m × 20 m, and
(c) 30 m × 30 m. Black arrows show significant ef-
-0.126*** fects; dotted arrows show nonsignificant effects. For
Soil P -0.08 *** Hillshade all paths, the standardized coefficients and sig-
7** 0.363
-0. nificance (*P < 0.05, **P < 0.01, ***P < 0.001)
23 **
6*
** 05 are given. Basal arealarge: the basal area of large trees;
0.1 species richnesslarge: the species richness of large
Stand densitysmall Species richnesssmall trees; basal areasmall: the basal area of small trees;
species richnesssmall: the species richness of small
0.1 trees. For more statistics from the structural equation
84 **
** 83 models, see Table S3.
* 0.0
-0.143*** 0.275***
LAI (R2 = 0.377)

(b) 20 m × 20 m
Basal arealarge Species richnesslarge
-0.25*** -0.169**

***
0.265
-0.13*
Soil P ** Hillshade
0.157
-0.
34
3*
**

Stand densitysmall Species richnesssmall

0.2 **
06 79
** 0.1
-0.183** 0.18**
LAI (R2 = 0.328)

(c) 30 m × 30 m
Basal arealarge Species richnesslarge
* *
89

*
.2

0.29*
-0

-0.236*
Soil P -0.22 Hillshade
3*
*
5*
27

-0.
36
0.

7*
**

Basal areasmall Species richnesssmall

0.2
3*
-0.239* 0.251**
LAI (R2 = 0.222)

2. Materials and methods
2.1. Study site
The study site is located within the Liangshui National Nature
Reserve of Northeast China (47.18° N, 128.89° E). The reserve covers a
12,133-ha area, with approximately 1.88 million m3 of growing stock
and an average canopy coverage of 98%. The altitude ranges from 280
to 707 m above sea level, with an average slope of 10–15°. The mean
annual air temperature is −0.3 °C, and the mean air temperature for
the summer season (from June to August) is 17.5 °C. The mean annual
precipitation is 676 mm, of which 10–20% is derived from snowfall.
The area is covered by snowpack from December through April (Liu
et al., 2015a). The study was conducted in a 9 ha (300 m × 300 m) old-
growth mixed broadleaved-Korean pine (Pinus koraiensis) forest dy-
namic plot in which the dominant species include Pinus koraiensis, Abies
nephrolepis, Tilia amurensis, Acer mono, Betula costata, and Fraxinus
mandshurica, and the species composition and shade tolerance of main
species refer to Liu et al. (2015b) and Niinemets & Valladares (2006).
2.2. Sampling design for LAI measurement
The LAI was measured at three scale levels, 10 m × 10 m,
20 m × 20 m and 30 m × 30 m, which resulted in 900, 225 and 100
subplots in the forest plot (9 ha). At the center of each subplot, the LAI
below the canopy was measured using a LAI-2200 plant canopy ana-
lyzer (PCA, LI-COR Inc., Lincoln, NE, USA) instrument under diffuse
light conditions. Another LAI-2200 PCA instrument was placed in a

3
Z. Liu, et al.
tower close to the study sites and automatically logged data every 15 s
to obtain the reference ‘above canopy’ data. A 90° view cap was used on
both ‘above canopy’ and ‘below canopy’ sensors to block any remaining
direct light and to avoid the influence of the operator on the sensor. The
sensor below the canopy measured diffuse sky radiation (320–490 nm)
at 1.3 m height above the ground in five zenith angle rings (i.e., 0–13°,
16°–28°, 32°–43°, 47°–58°, and 61°–74°) (LI-COR, 1992). The potential
area ‘seen’ by the sensor is a circle with a radius of tan(θ) × (h − 1.3)
m, where θ is the zenith angle and h is the height of the forest canopy,
which has a mean value of 20 m in this forest plot. Thus, the radii for
the 15°, 30° and 45° zenith angles are 5 m, 10 m and 18 m, respectively.
To reasonably measure the LAI value for each sample point, 1, 1–2 and
1–3 rings that cover zenith angle ranges of approximately 0–15°, 0–30°
and 0–45° were selected to calculate the stand LAI in the 10 m × 10 m,
20 m × 20 m and 30 m × 30 m plots, respectively.
However, the LAI estimated directly from optical methods (e.g., the
LAI-2200) usually needs to be corrected; because optical methods can
overestimate the LAI by mistaking woody materials for leaves and can
underestimate the LAI by ignoring clumping effects within canopies,
especially for coniferous species, which show beyond-shoot and within-
shoot clumping effects (Chen et al., 1997). To obtain more accurate LAI
values, we corrected the LAI from LAI-2200 using the following
method. We corrected the error caused by woody materials by using the
woody-to-total area ratio (Chen, 1996; Leblanc et al., 2005), which was
estimated by the digital hemispherical photography method (Liu et al.,
2015a). The error caused by ignoring beyond-shoot clumping effects
was corrected by the clumping index, which was calculated based on
the canopy gap size distribution theory (Chen & Cihlar, 1995; Leblanc
et al., 2005). The error caused by ignoring within-shoot clumping ef-
fects was corrected by the needle-to-shoot area ratio, which was mea-
sured by weighting the needle-to-shoot area ratios of the trees of dif-
ferent species by their relative contributions to the total basal area in
the grid cell. For the details of calculating these three parameters, refer
to Liu et al. (2015a). In this case, the LAI values used in this study were
all corrected.
2.3. Measurement of biotic and abiotic factors
The biotic factors that were determined for each subplot included
stand structure and species richness. The stand structure included stand
density, basal area and mean DBH. For each 10 m × 10 m,
20 m × 20 m and 30 m × 30 m quadrat, all individuals with
DBH ≥ 1 cm were recorded. To evaluate the effects of tree size on LAI,
we divided all individuals into two groups: large trees with
DBH > 9 cm and small trees with DBH ≤ 9 cm (Zhang et al., 2017).
Then, we calculated the stand density, basal area, mean DBH and
species richness for both large trees and small trees in each quadrat at
10 m × 10 m, 20 m × 20 m and 30 m × 30 m scales.
The abiotic factors were divided into two groups, i.e., soil properties
and topography. The soil properties that were determined for each
quadrat included soil pH, total N content, total P content and mass
moisture. A combination of systematic and random sampling methods
was used to collect soil samples at 0–10 cm soil depth (see Fig. 2 in Shi
et al., 2016). At the intersections of a 20 m × 20 m grid, 256 samples
were collected, and two additional sample points (2, 5 or 8 m) were
then selected in a random direction from the intersections. Thus, a total
of 768 locations were sampled in our 9 ha forest plot (Shi et al., 2016).
The values of the soil properties that were measured in the
20 m × 20 m grid were interpolated to those for a 5 m × 5 m grid with
ordinary kriging, and then these variables were calculated for larger
cells (i.e., 10 m × 10 m, 20 m × 20 m and 30 m × 30 m) based on the
mean values of the 5 m × 5 m cells contained within each larger cell.
Elevation is one of most commonly used topographic variables in
determining the distribution of LAI because elevation is closely related
not only to temperature but also to light and soil conditions
(Spadavecchia et al., 2008; Xu et al., 2015). However, here, we aim to
4
Forest Ecology and Management 479 (2021) 118540
separately evaluate the influence of each of temperature, light and soil
on LAI variations. First, the elevation change in this forest plot is less
than 71 m, and the corresponding temperature difference is less than
0.4 °C (approximately 0.6 °C per 100 m) (Spadavecchia et al., 2008);
thus, we assume that the effect of temperature on LAI variation is
minimal. Additionally, we measured the soil properties (soil nutrients
and soil water) in each subplot; thus, the elevation was not considered
in this study. Rather, the topographic variable that was used for each
quadrat was the hillshade. Researchers have often used slope and aspect
to characterize the relative light intensity in previous studies, regardless
of the solar altitude and azimuth. The aspect and mean annual solar
azimuth can be combined to determine the shady or sunny status of
slopes, and the slope and annual mean solar altitude may affect the
light intensity on shady slopes depending on whether the slope is less
than the solar altitude. However, hillshade, which is based on an overall
consideration of aspect, slope, mean annual solar azimuth and altitude
(or zenith) (Burrough & McDonell, 1998), can be used to characterize
the relative illumination intensity at a specific location. Thus, we used
hillshade to describe the light availability in each quadrat. We created
10-m, 20-m and 30-m raster DEM data based on contour (interval: 1 m)
polyline vector data (ESRI Shapefile) in ArcGIS 10.1. Then, we calcu-
lated 10-m-, 20-m- and 30-m-scale hillshades based on the DEM data at
the corresponding scale. The mean annual solar azimuth and altitude in
our plot were approximately 202.5° and 45°, respectively.
2.4. Data analysis
We developed a conceptual model (Fig. 1). The LAI is potentially
directly influenced by two types of biotic factors (stand structure and
species richness) for large trees and small trees and two types of abiotic
factors (soil properties and topography). We also considered indirect
effects, e.g., abiotic factors that potentially influence biotic factors and
that the stand structure and species richness of small trees are influ-
enced by those of large trees. To analyze their contributions, we used
structural equation modeling (SEM). Although we had more than two
possible candidate variables for stand structure for both large trees and
small trees and soil properties, we could only include one variable at a
time in the SEMs. To reduce the number of variables for each factor and
thus the number of possible SEMs to choose from, we used multiple
regression analyses to preselect the variable with the highest relative
variable importance (Barton, 2015) at each scale (Table S1). Then, we
performed an all-subset regression analysis for the candidate variables
per factor for LAI following van der Sande et al. (2017), which was
expected to lead to 2 (stand structure for large trees) × 1 (species
richness for large trees) × 2 (stand structure for small trees) × 1
(species richness for small trees) × 2 (soil properties) × 1 (hill-
shade) = 8 possible SEMs for each scale.
Then, the performance of the SEMs was evaluated using a combi-
nation of the chi-square statistic (where P > 0.05 indicates a good
model fit), Bentler’s comparative fit index (CFI, where CFI ≈ 1 in-
dicates a good model fit) and the standardized root mean square re-
sidual (SRMR, where SRMR ≤ 0.05 indicates a good model fit) (Hoyle,
2012; Yuan et al., 2019). Finally, for the SEMs for LAI at each scale, we
selected the best SEM with P > 0.05, CFI > 0.95 and SRMR < 0.05
and the highest explained variation (R2) (Table S2). The indirect effect
of a predictor was calculated by multiplying the coefficients of all paths
linking the exogenous variables to each LAI, while the total effect was
obtained by summating the standardized direct and indirect coefficients
(Ali et al., 2019b; Yuan et al., 2019).
The relative contribution of each predictor to the explained variance
in the LAI was calculated as the ratio between its parameter estimate
(standardized regression coefficients) and the sum of all parameter
estimates (Le Bagousse-Pinguet et al., 2017). Prior to analysis, the LAI
values were log-transformed to meet the assumptions of equal variances
and normal distribution of residuals. All analyses were performed in R
3.4.2 (R Core Team, 2017). All subset regression analyses were
Z. Liu, et al. Forest Ecology and Management 479 (2021) 118540

Table 1
Descriptive statistics of LAI, biotic factors (stand structure and species richness) for large trees (DBH > 9 cm) and small trees (DBH ≤ 9 cm), soil properties, and
topography (hillshade) at three scale levels (10 m × 10 m, 20 m × 20 m, and 30 m × 30 m) in a mixed broadleaved-Korean pine forest plot.
Parameters Variable Unit 10 m × 10 m 20 m × 20 m 30 m × 30 m

Max Min Mean SD Max Min Mean SD Max Min Mean SD

Response LAI m2/m2 15.4 1.4 7.4 2.8 9.6 6 7.8 0.7 11.4 4.1 7.6 1.6
Large tree Stand density N/ha 1400 100 417 202 1025 150 408 123 800 233 408 101
Basal area m2/ha 176.5 0.7 37 30 83.5 6 35.5 13.8 64.4 15.7 35.1 9.8
DBH cm 86.4 9.1 28.2 10.9 50.2 14.9 28.1 5.4 36.4 17.1 27.9 4.1
Species richness No. of species 7 1 3 3 8 1 4 1 18 5 10 2

Small tree Stand density N/ha 9900 400 3286 1759 6325 1225 3278 1115 5444 1789 3296 842
Basal area m2/ha 7.23 0.15 1.86 1.02 3.71 0.65 1.87 0.67 3.58 0.87 1.88 0.55
DBH cm 5.3 1.4 2.3 0.6 4.1 1.7 2.3 0.4 3.3 1.7 2.3 0.3
Species richness No. of species 13 2 7 2 15 5 9 2 27 14 19 3

Soil properties pH – 6.3 5.3 5.8 0.2 6.2 5.4 5.8 0.2 6.2 5.5 5.8 0.1
Total N mg/g 12.3 4.6 8.4 1.6 11.9 4.9 8.4 1.6 11.7 5.1 8.4 1.5
Total P mg/g 1.22 0.41 0.82 0.15 1.17 0.42 0.82 0.15 1.13 0.44 0.82 0.14
Mass Moisture g/g 1.51 0.54 0.92 0.23 1.44 0.55 0.92 0.23 1.4 0.55 0.91 0.22
Topography Hillshade 248 140 192 20 233 155 195 13 226 168 195 9

performed using the MuMIn package. Linear models were evaluated had a positive effect on species richnesslarge (Fig. 2c); basal arealarge had
using the lm function. Structural equation modeling was performed a negative effect on basal areasmall but species richnesslarge had a po-
using the sem function of the lavaan package. sitive effect on basal areasmall (Fig. 2c).

3. Results
3.1. Effects of biotic and abiotic factors on LAI
Table 1 summarizes the statistical information for LAI and all pre-
dictors. The best predictors of LAI varied slightly among the three scales
(Fig. 2, Table S2). For large trees (DBH > 9 cm), the basal area was
always selected to describe stand structure at the three scales. In con-
trast, stand density was selected to describe stand structure at the
10 m × 10 m and 20 m × 20 m scales for small trees (DBH ≤ 9 cm),
but basal area was selected at the 30 m × 30 m scale (Fig. 2, Table S2).
For soil properties, soil P was selected at the 10 m × 10 m,
20 m × 20 m and 30 m × 30 m scales. The total variations in the LAI
explained by all factors considered here decreased with increasing
scale, i.e., with R2 values of 0.377, 0.328 and 0.222 at the
10 m × 10 m, 20 m × 20 m and 30 m × 30 m scales, respectively
(Fig. 2).
At the 10 m × 10 m scale, basal arealarge had a direct negative effect
on the LAI (Fig. 2) and indirectly reduced the LAI by decreasing stand
densitysmall (Tables S3 and S4). Both stand densitysmall and species
richnesssmall had direct positive effects on the LAI (Fig. 2). Soil P had a
direct negative effect on the LAI (Fig. 2a) and indirectly reduced the LAI
by affecting stand densitysmall and species richnesssmall (Tables S3 and
S4). Hillshade had a direct positive effect on the LAI (Fig. 2a) and in-
directly enhanced the LAI by increasing stand densitysmall (Tables S3
and S4).
At the 20 m × 20 m scale, both basal arealarge and species rich-
nesslarge had direct negative effects on the LAI, but both stand densi-
tysmall and species richnesssmall had direct positive effects on the LAI
(Fig. 2b). Soil P had a direct negative effect on the LAI (Fig. 2b) and
indirectly reduced the LAI by affecting species richnesslarge and stand
densitysmall (Tables S3 and S4). Hillshade had a direct positive effect on
the LAI (Fig. 2b) and indirectly enhanced the LAI by increasing stand
densitysmall (Tables S3 and S4).
At the 30 m × 30 m scale, unexpectedly, among all biotic factors for
large trees and small trees, only basal areasmall had a direct positive
effect on the LAI (Fig. 2c; Tables S3 and S4). Soil P had a direct negative
effect on the LAI (Fig. 2c) and indirectly reduced the LAI by decreasing
the basal area of small trees (Tables S3 and S4). Hillshade had a direct
positive effect on the LAI (Fig. 2c). In addition, soil P had negative
effects on basal arealarge, basal areasmall and species richnesssmall and
3.2. Relative contributions of biotic and abiotic factors to the variation in
the LAI
The contributions of these biotic and abiotic factors to the variation
in LAI clearly varied with scale (Fig. 3). At the 10 m × 10 m scale, stand
structurelarge made the largest contribution (30.2%) to the variation in
the LAI, followed by those of hillshade (29.9%); soil property (17.3%)
and stand structuresmall (15.1%) made similar contributions to the
variation in the LAI; and species richnesssmall and species richnesslarge
made relatively small contributions to the variation in the LAI (Fig. 3).
At the 20 m × 20 m scale, soil properties (21.1%) made the largest
contribution to the variation in the LAI, followed by that of stand
structurelarge (21.0%), and the contributions of other factors to the
variations in LAI were similar, ranging from 11.8% to 18.5% (Fig. 3). At
the 30 m × 30 m scale, soil property made the largest contribution
(27.7%) to the variation in the LAI, followed by those of hillshade
(25.3%) and stand structuresmall (22.4%), and species richnesssmall and
stand structurelarge made relatively small contributions to the variation
in the LAI (Fig. 3).
In general, the total contributions (both stand structure and species
richness) of large trees to LAI variation decreased with increasing scale
but increased for small trees, and the total contributions of large trees at
the small scale (e.g., 10 m × 10 m) were greater than those of small
trees at the small scale but lower than those of small trees at the large
scale (e.g., 30 m × 30 m) (Fig. 3). In addition, the contribution of the
direct effect of stand structurelarge decreased with increasing scale but
the contribution of its indirect effect increased with increasing scale
(Fig. 4). The contributions of the direct effects of soil properties on LAI
variations increased with increasing scale; and the contribution of the
indirect effect of hillshade decreased with increasing scale (Fig. 4).
4. Discussion
In this study, we evaluated the influences of stand structure and
species richness in large and small trees, soil properties and light (i.e.,
hillshade) on the LAI in different plot sizes in a natural forest. We found
that the basal area of large trees directly reduced the LAI at the smaller
plot sizes but had no influence at the largest scale; the stand density or
basal area of small trees always enhanced the LAI at the different plot
sizes. The species richness of small trees enhanced the LAI at
10 m × 10 m and 20 m × 20 m; in contrast, the species richness of

5
Z. Liu, et al. Forest Ecology and Management 479 (2021) 118540

10 m × 10 m 20 m × 20 m 30 m × 30 m
2.3
Stand
SS structure
for large tree large
18.5 21.0 15.7
25.3
Relative contribution (%)

29.9 30.2 SR for large

Species tree large
richness

SS for small
Stand treesmall
structure
11.8
21.1 22.4 Species
SR richness
for small treesmall
0.7
Soilproperty
Soil property
17.3 15.1 27.7
14.7
6.8 12.8 6.6 Hillshade
Hillshade

35
10 m × 10 m 20 m × 20 m 30 m × 30 m
30
Relative contribution (%)

25

20

15

10

0
Large tree Small tree Soil property Hillshade

Fig. 3. Relative contributions of biotic factors (stand structure and species richness for large trees and small trees separately) and abiotic factors (soil properties and
hillshade) to LAI variations at three sampling scales: 10 m × 10 m, 20 m × 20 m, and 30 m × 30 m. Relative contribution of large trees (or small trees) to the LAI
was the sum relative contributions of both stand structure and species richness of large trees (or small trees) to the LAI.

large trees only significantly reduced the LAI at 20 m × 20 m. The
hillshade always enhanced the LAI, but soil P always reduced the LAI at
the different plot sizes. Interestingly, the contributions of large trees to
the LAI decreased with increasing plot size, but those of small trees
increased, and the contributions of soil properties to the LAI increased
with increasing plot size, but hillshade made more contributions to the
LAI at smaller plot sizes.
In the smallest (10 m × 10 m) and intermediate (20 m × 20 m) plot
sizes, the basal area of large trees had strong direct negative effects on
the LAI in the natural forest, which supports our first hypothesis.
Although the LAI of a large tree is generally higher than that of a small
tree at the individual scale, as the tree grows, the tree allocates more
biomass to the trunk than to the leaves to protect itself from external
damage (e.g., wind or rainstorms) (Meinzer et al., 2011); in this case,
the LAI increases first and then stabilizes as the tree grows. Ad-
ditionally, the high basal area in a stand is mostly contributed by a few
large trees in a natural forest, but these large trees not only intercept
most of the light energy but also have a stronger absorption capacity for
soil nutrients and moisture than small trees, thereby limiting the sur-
vival and growth of small trees (Légaré et al., 2005; Bartels & Chen,
2013; Zhang et al., 2017; Ali et al., 2019a) and reducing the LAI at the
stand level. This phenomenon is supported by the fact that the basal
area of large trees indirectly decreased stand LAI by limiting the stand
density of small trees (Table S4). However, in the largest plot size
(30 m × 30 m), the basal area of large trees had no effect on the LAI;
this finding supports our third hypothesis that the contributions of large
trees to the LAI decline with increasing plot size (Fig. 3). This is
probably because the plot size is larger than the area of resource control
of a large tree; in an area of this size, the survival and growth of other
small trees increase, thus weakening the contribution of the large tree
to the LAI (Borders et al., 2008; Sambakhe et al., 2014).
As expected, the basal area of small trees had direct effects on the
LAI at the three plot sizes, probably because the basal area is closely
and positively related to leaf biomass (Paquette & Messier, 2010;
Temesgen et al., 2011; Chave et al., 2014; Stephenson et al., 2014;
Ishihara et al., 2015). The basal area of large trees indirectly reduced
the LAI by limiting the basal area or stand density of small trees at the
10 m × 10 m scale, again confirming the positive contributions of the
basal area of small trees to the stand LAI. Additionally, the contribu-
tions of small trees to the LAI increased with increasing plot size and
were larger than those of large trees at the largest plot size, but the
opposite result was observed at the smallest plot size (Fig. 3), which
supports our first hypothesis. These results again confirm the dominant
effects of large trees on the stand LAI at the small scale (Slik et al., 2013;
Ali et al., 2019b); large tree factors explained more than 30% of the
total variation in the LAI at the 10 m × 10 m scale. Therefore, plot size
plays a key role in exploring the influences of biotic factors for both
large trees and small trees on the LAI. In addition, at the 30 m × 30 m
scale, the species richness of large trees had direct positive effects on
the basal area of small trees, probably because a high diversity of large
trees may enhance the resource heterogeneity and availability for small
trees through light penetration and litterfall feedback, which in turn
promote the growth of small trees (Bartels & Chen, 2013; Zhang et al.,
2017).
Unexpectedly, soil nutrients, i.e., soil P, had strong direct negative
effects on the LAI at the three plot sizes (Fig. 2). It is often reported that
forests with high soil nutrients support many more species (i.e., have
high species richness) due to their greater niche-axis length (Coomes
et al., 2009; Yuan et al., 2019). Large trees usually have better access to
soil resources because they have large root systems that can efficiently
absorb these resources (Meinzer et al., 2011; Ali et al., 2019a). This
may be why the soil nutrient level was positively correlated with spe-
cies richness for large trees (Fig. 2b, c). However, at the same time, high
soil nutrition may lead to better total growth, and then probably lead to
stronger competition, resulting in higher tree mortality and thus lower
LAI (Fig. 2b) (Quesada et al., 2012). This may also be the reason for the
negative correlations between soil nutrients and basal area for large
trees (Fig. 2c). However, large trees may effectively take up large

6
Z. Liu, et al. Forest Ecology and Management 479 (2021) 118540

Stand structurelarge Species richnesslarge Stand structuresmall 2016). In addition, our results highlight that plot size effects should be
Species richnesssmall Soil property Hillshade seriously considered when exploring the relationships between soil
nutrient levels and biotic factors.
Hillshade (as a proxy of light availability) enhanced the stand LAI at
all different plot sizes, mainly because light is an important limiting
factor for plant growth (Rüger et al., 2012; Coble et al., 2017; Poorter
et al., 2019; Velázquez & Wiegand, 2020). In particular, high light
availability clearly enhances regeneration and growth for small trees
(King et al., 2010; Meinzer et al., 2011; Rüger et al., 2012; Danescu
et al., 2016). These findings are also supported by our results, i.e.,
hillshade indirectly enhanced the stand LAI by increasing the stand
density at the 10 m × 10 m scale and by increasing the stand density of
small trees at the 20 m × 20 m scale. In contrast, as trees grow, the
enhancement effect of light on tree growth gradually weakens, and
10 m 10 m
when the trees enter the forest canopy layer, light is no longer the
-0.5 -0.3 -0.1 0.1 0.3 0.5 limiting factor for tree growth (Coleman et al., 1994; Woodruff et al.,
2010; Meinzer et al., 2011). This case is supported by our results, i.e.,
hillshade had no influence on the biotic factors of large trees at any plot
size (Fig. 2).
Scale effects have long been a focus of investigation in forest
ecology because the influences of biotic factors and abiotic factors on
tree performance or community assembly vary markedly with spatial
scale (Spadavecchia et al., 2008; Xu et al., 2009; Chave, 2013; Yan
et al., 2016). Biotic interactions are likely to be more important in the
composition of tree assemblages at fine spatial scales, whereas abiotic
filtering is typically more important at larger spatial scales (Yang et al.,
2014; Yuan et al., 2016). This case is generally supported by our finding
that the contributions of biotic factors to LAI variation (varying with
20 m 20 m tree performance) are larger than those of abiotic factors at smaller
scales (e.g., 10 m × 10 m), but the opposite result occurred at larger
-0.5 -0.3 -0.1 0.1 0.3 0.5
scales (e.g., 30 m × 30 m). Additionally, at smaller scales, the con-
tribution of soil nutrients to stand LAI was lower than that of hillshade,
but at the larger scale, the opposite result occurred, indicating that light
is more important in driving tree growth (or LAI) at the small scale, but
soil properties are more important at the large scale. This may be be-
cause the heterogeneity of soil nutrients is greater at large scales and
thus supports more individuals (Webster, 1985; Shi et al., 2016), but
the heterogeneity of light availability is likely to show the opposite
trend. The inconsistent heterogeneity of these abiotic factors probably
drives the spatial distribution of species and thus LAI, which supported
by differences of variations (SD) of the LAI at different plot sizes
(Table 1).
30 m 30 m
5. Conclusions
-0.5 -0.3 -0.1 0.1 0.3 0.5
Parameters estimated In summary, our study provided evidence that scale plays a key role
in revealing the contributions of both biotic and abiotic factors to LAI
Fig. 4. Parameter estimates (standardized regression coefficients) on the LAI at variation at the local scale. The basal area of large trees with DBH
three sampling scales: 10 m × 10 m, 20 m × 20 m, and 30 m × 30 m. The values larger than 9 cm directly limited the LAI at all three scales
filled bars indicate the direct effects, and the slash lines indicate the indirect
(10 m × 10 m, 20 m × 20 m and 30 m × 30 m) and indirectly limited
effects of stand structure and species richness of large trees, soil properties and
the LAI by decreasing the growth of small trees with DBH values lower
hillshade on the LAI.
than 9 cm, but the species richness of the large trees had less influence
on the LAI. In contrast, the stand structure (e.g., basal area and stand
amounts of local soil nutrients and reduce resource availability for density) of small trees enhanced the LAI at all scales, and similar results
small trees (Bartels & Chen, 2013; Ali et al., 2019a). In this case, re- were shown for the species richness of small trees. These results high-
source filtering would increase the species complementarity effect light the importance of tree size in driving stand LAI variation. Soil
under low soil nutrient conditions (Zhang et al., 2017) where the stand properties and light (represented by hillshade) all had strong direct
structure or species richness of small trees promotes stand LAI, probably effects on stand LAI at the three scales but showed opposite contribu-
due to the competitive constraints caused by the large trees (Bartels & tion patterns. Interestingly, we also found that the contribution of large
Chen, 2010; Zhang et al., 2017). These opposing effects of soil nutrients trees (the sum of stand structure and species richness) to stand LAI was
on stand structure and species richness between large trees and small higher at the small scale than that at the large scale, but the con-
trees may largely explain the observed direct negative effects of soil tribution of small trees (the sum of stand structure and species richness)
nutrients on stand LAI. On the other hand, the negative relationships to stand LAI increased with increasing scale. The contribution of soil
between soil nutrients and stand LAI may be attributable to species properties to the LAI increased with increasing scale, but light con-
adaptations to the local soil conditions through increased longevity and tributed more to the LAI at smaller scales. These results suggest that the
stand biomass retention (Poorter et al., 2015; Prado-Junior et al., mechanisms that drive the influences of biotic factors and abiotic

7
Z. Liu, et al.
factors on stand LAI are diverse and that their relative importance de-
pends on scale. Therefore, tree size and scale effects should be in-
tegrated in further studies of running LAI-based models, such as forest
carbon cycle models and global vegetation growth dynamics models.
6. Author statement
The manuscript is original, was not submitted to any other journal,
and was approved by all authors.
Author contributions
ZL Liu and GZ Jin planned and designed the research. ZL Liu per-
formed experiments and conducted fieldwork. ZL Liu and B Li analysed
data and wrote the manuscript. GZ Jin provided helpful comments in
the draft.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgment
The work was financially supported by the National Natural Science
Foundation of China (No. 31971636 and 31870399) and the
Heilongjiang Touyan Innovation Team Program for Forest Ecology and
Conservation. We also would like to thank the responsible editor and
the anonymous reviewers for their constructive and helpful comments
that helped to improve the manuscript.
Appendix A. Supplementary material
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.foreco.2020.118540.
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