J. Mt. Sci. (2015) 12(3): 659-670 e-mail: jms@imde.ac.cn http://jms.imde.ac.

cn
DOI: 10.1007/s11629-013-2795-1

Distribution Patterns and Associations of Dominant Tree

Species in a Mixed Coniferous-Broadleaf Forest in the
Changbai Mountains

ZHANG Meng-tao1, http://orcid.org/0000-0002-4152-1019; e-mail: zmt0411@163.com

KANG Xin-gang1, http://orcid.org/0000-0002-9284-255X; e-mail: kxg520512@163.com

MENG Jing-hui1, http://orcid.org/0000-0002-1548-7486; e-mail: jmeng@bjfu.edu.cn

ZHANG Li-xin2, http://orcid.org/0000-0001-9761-0590; e-mail: 534259627@qq.com

1 Key Laboratory for Silviculture and Conservation Ministry of Education, Beijing Forestry University, Beijing 100083,
China
2 Yunnan Forest Institute, Kunming 650204, China

Citation: Zhang MT, Kang XG, Meng JH, et al. (2015) Distribution patterns and associations of dominant tree species in
a mixed coniferous-broadleaf forest in the Changbai Mountains. Journal of Mountain Science 12(3). DOI: 10.1007/s11629-
013-2795-1

© Science Press and Institute of Mountain Hazards and Environment, CAS and Springer-Verlag Berlin Heidelberg 2015

Abstract: In 2012 a plot was established with 1-ha
area in a mixed coniferous-broadleaf forest in the
Changbai Mountains, northeastern China for
examining local forest processes, structure and
succession. A method of O-ring statistics (pair-
correlation function) was applied to analyze the
spatial patterns and associations of the dominant
species within different vertical layers. After the
evaluation by their importance values, six tree species
(or group) (i.e. Abies nephrolepis, Picea jezoensis,
Pinus koraiensis, Tilia amurensis, and species group
of Betula ssp. and species group of Acer ssp.) were
determined as dominant trees species. It was found
that some of these species exhibited closely clustered
distributions at fine distances. As spatial distance
increased, a random or even regular distribution
gradually appeared with the exception of the upper
layers of A. nephrolepis and P. koraiensis, and the
lower layers of P. jezoensis, P. koraiensis and Betula
ssp., which were substantially randomly distributed.
Intra- and inter-species spatial associations varied in
accordance with species, tree height and reciprocal
distances. Positive associations were observed
Received: 5 November 2013
Accepted: 14 May 2014
between the lower and upper height classes of trees of
the same species (except for that of P. jezoensis) at
fine distances. This may be owing to limited seed
dispersal and geological heterogeneity. The
aggregation intensity declines with increasing
distances and this consistent with the predictions of
self-thinning. Some coniferous trees (e.g. Pinus
koraiensis) in the lower height class were positively
associated with T. amurensis and group of Betula ssp.
of the upper height class at some distances, suggesting
that saplings of coniferous trees occupy a broader
niche and can grow well under the canopy of the adult
of broad-leaved trees. Negative associations were
observed between upper coniferous trees and lower
broad-leaved trees and between upper P. jezoensis and
lower P. koraiensis, suggesting that a canopy of these
trees might not provide suitable environment for the
survival, establishment, and growth of lower
individuals, corresponding well to Janzen-Connell
hypothesis.
Keywords: Mixed coniferous-broadleaf forest; O-
ring statistics; Spatial pattern; Spatial association;
Null model

659
J. Mt. Sci.(2015) 12(3): 659-670
Introduction
Most natural systems are spatially non-
homogeneous. Instead, they usually exhibit
different sorts of spatial structure (Dale et al.
2002). Forest spatial structure is defined as the
distribution pattern of individual trees and the
spatial arrangement of forest attributes (Hui and
Gadow 2003; Larson and Churchill 2012). The
spatial patterns of trees and their interactions
provide critical information on community
structure and species coexistence as well as
significantly determine reproduction, growth,
mortality, dispersal, resource use, gap creation,
and understory development (Wiegand et al. 2007a;
Zhang et al. 2010). The study of vertical structure
plays an important role in the understanding of
forest ecosystems, since the spatial structure of a
community is closely related to diverse processes
and drivers including intra- and interspecific
competition, seed dispersal, disturbance, and
environmental heterogeneity (Condit et al. 2000;
Stoyan and Penttinen 2000; Zhang 2004). The
analysis of spatial patterns based on different tree
height classes can supply important information
for the measurement of population characteristics
and the relationship between population and
environment (Druckenbrod et al. 2005; Manabe et
al. 2000; Paluch 2007).
Mixed coniferous-broadleaf forest is the
dominant forest type in the Changbai Mountains
and such forest generally exhibits high species
richness and a distinctive species composition
(Stone 2006). The environment in these forested
lands provides suitable habitat for many rare
species (Shao et al. 1994). Thus, understanding the
biological characteristics of component species and
the potential ecological processes functioning
within this forest is pivotal. In recent years, many
studies for this type of forest have mainly focused
on tree or stand growth using simulation models
(Peng 2000), allocation of forest biomass (Wang
2006) and regeneration (Wang and Liu 2011).
Several studies have reported varying results
concerning forest spatial structure. For example,
Lei et al. (2007) used Ripley’s K (L) function to
examine the spatial structure of a semi-natural
larch-spruce-fir forest based on data collected from
stands subjected to different thinning intensities
between 1987 and 1999. Their results indicate that
660
different species were randomly distributed at the
2–3 m distance and clustered at other distances.
Gong et al. (2010) used three spatial structure
parameters, mingling degree, neighborhood
comparison, and the uniform angle index, to
analyze the succession of spatial structure in a
spruce-fir mixed forest in the Changbai Mountains
from 1989 to 2005, and demonstrated that the
spatial pattern of the stand shifted from a random
distribution in 1989 to a slightly clumpy
distribution in 2005. Fajardo et al. (2006)
investigated spatial patterns and associations
between saplings and overstory trees using Ripley’s
L function in 11 plots (20 m × 30 m). The trees
exhibited obvious aggregated distributions.
Moreover, bivariate associations were observed
between saplings of both study species and
overstory trees, and both positive and negative
spatial associations occurred depending on the plot.
In general, these studies on mixed forests reported
horizontal heterogeneity of spatial patterns and
associations using Ripley’s K (L) function. However,
few studies have examined the spatial structure of
different forest layers, especially for the mixed
forests of high structural complexity in the early-
successional stages of development.
The method of O-ring statistics has been
widely used in the field of ecology (Riginos et al.
2005; Stoyan and Penttinen 2000; Wiegand and
Moloney 2004; Xu et al. 2009). In this study, we
analyzed the spatial patterns and intra- and
interspecies spatial associations within different
vertical layers in a 1-ha mixed coniferous-broadleaf
forest using O-ring statistics. We assumed that: (i)
trees are aggregated at fine distances due to limited
seed dispersal ability, but with increasing distance
between individuals, distributions are random or
even regular; (ii) there are positive or negative
associations between species pairs at fine distances,
but species distributions are independent at coarse
distances; (iii) distance between trees is an
important ecological parameter. We examined
these assumptions by (1) evaluating the spatial
patterns of dominant tree species and examining
the intra- and interspecies spatial associations
among different tree height classes in the forest; (2)
verifying the relationship between species and
competition among different species; and (3)
determining the role of vertical structure in the
succession of a mixed coniferous-broadleaf forest.
 J. Mt. Sci.(2015) 12(3): 659-670

1 Methods gridded by their geographic coordinates (x, y). All

1.1 Study Area
The study site was randomly established
within an uneven-aged mixed coniferous-broadleaf
forest in its early-successional stages of
development in the Changbai Mountains at the Jin
Gouling Bureau, Wangqing, in northeastern China
(43°22'N, 130°10'E) (Lei et al. 2007). The area
exhibits the marine-type characteristics of a
temperate monsoon climate (Zhang et al. 2012).
The monthly mean temperature is 3.9°C, and the
accumulated temperature above 10°C is about
2473°C. Annual precipitation is 500–600 mm, and
the frost-free duration is 110–130 days. The region
has 170 days of snow fall in the period between
November and April; this form of precipitation is
the dominant “natural disturbance” (Li et al. 2013).
The soil is a brown podzol type. The elevation of
the study plot is 700 m, and gradient is 3°–5°. The
mean age of overstory trees is about 70 years. The
main tree species include Pinus koraiensis Sieb. et
Zucc., Picea jezoensis Carr., Abies nephrolepis
(Trautv.) Maxim., and Tilia amurensis Rupr.; other
species include Betula platyphylla Suk. and Acer
mono Maxim.
1.2 Data Collection
The 1-ha plot was laid and then divided into 25
subplots (20 m × 20 m). Within each subplot, all
free-standing trees at least 5 cm in diameter at
breast height (DBH, 1.3 m above the ground) were
the trees were identified by their scientific name
and their DBH, locations and heights were
recorded. We combined Betula costata Trautv. and
Betula platyphylla Suk. as a group (Betula ssp.),
and combined Acer mono Maxim., Acer
tegmentosum Maxim. and Acer ukurunduense
Trautv. et as a group (Acer ssp.) because of they are
of the same genus, play similar ecological roles and
had fewer individuals. The total number of living
tree individuals in this census was 1313 comprising
12 species (or group) (Table 1).
1.3 Data Analysis
The importance value (IV) is a comprehensive
quantitative indicator used to characterize the
status and role of each species in a community. The
larger the IV of a tree species is, the greater its
dominance in the plot. It is calculated as follows:
(Rde+Rfr+Rdo )
Importance value (IV) = %
3
where Rde (Relative density) is the ratio of number
of individuals of a species and total number of
individuals; Rfr (Relative frequency) is the ratio of
frequency of a species and sum of frequencies of all
species; and Rdo (Relative dominance) is the ratio
of basal area of a species and total basal area of all
the species.
To analyze forest spatial structure, tree height
was used as a vertical measure because it is more
sensitive to ecological processes than other
parameters (Chen and Bradshaw 1999; Salas et al.
2006). We subsequently divided the vegetation

Table 1 Basic characteristics of tree species in a 1-ha mixed coniferous-broadleaf forest plot
DBH (cm)
Species Number of trees SD B-area I-Value
Max. Mean
Abies nephrolepis (Trautv.) Maxim. 463 45.2 16.3 9.073 12.726 0.59
Picea jezoensis Carr. 154 48.3 19.9 10.727 6.157 0.43
Species group of Acer ssp.* 256 37.5 10 4.958 4.345 0.43
Species group of Betula ssp.# 214 34.3 12.8 6.251 1.785 0.42
Pinus koraiensis Sieb. et Zucc. 94 55.5 21.1 12.062 3.387 0.38
Tilia amurensis Rupr. 121 42 11.6 7.255 2.507 0.37
Phellodendron amurense Rupr. 4 18.6 15.2 3.47 0.073 0.04
Populus davidiana Dode 3 30.4 19 9.947 0.085 0.04
Taxus chinensis (Pilger) Rehd. 1 - - - 0.011 0.01
Quercus mongolica Fis. ex Lede. 1 - - - 0.008 0.01
Fraxinus mandschurica Rupr. 1 - - - 0.006 0.01
Ulmus japonica Linn. 1 - - - 0.002 0.01
Notes: DBH = diameter at breast height; SD = Standard deviation; B-area = Basal area (m2/ha); I-Value =
Importance value; *Species group of Acer ssp. include Acer mono Maxim., Acer tegmentosum Maxim. and Acer
ukurunduense Trautv. et; #Species group of Betula ssp. include Betula costata Trautv. and Betula platyphylla Suk.

661
J. Mt. Sci.(2015) 12(3): 659-670
into different vertical layers by tree heights (Hao et
al. 2007; Zhang et al. 2007).
Spatial point pattern analysis procedures, such
as Ripley’s K function and O-ring statistics (pair-
correlation function), are commonly applied to
detect the spatial arrangement of individuals
within communities and to generate hypotheses
about the underlying processes that control the
patterns observed (Ripley 1981; Stoyan and Stoyan
1994; Wiegand et al. 2007b). However, some
pitfalls may occur when Ripley’s K is used for
analysis of spatial patterns because the analysis of
Ripley’s K function provides information for a
range of distances. With increases in radius, results
at coarser distances include information at finer
distances within the circle. O-ring statistics can
effectively rule out the influence of cumulative
effects; they are developed from Ripley’s K function
by replacing the circles of Ripley’s K function with
rings, which can isolate specific distance classes
and analyze spatial patterns at a given distance r
(Fortin and Dale 2005; Hao et al. 2007; Xu et al.
2009; Zhang et al. 2009). O-ring statistics include
both univariate and bivariate procedures.
Univariate statistical procedures are used to
analyze the spatial pattern of a single object.
Bivariate methods are used to analyze the spatial
association of two objects. In our study, univariate
statistics were used to analyze the distribution of
dominant tree species in different vertical layers.
We then examined intra- and interspecies
correlations using a bivariate statistic. We used
Poisson cluster models (Thomas process), which
take into account of possible clustering
mechanisms, to reveal uni- and bivariate
interactions and then followed procedures
described by Perry et al. (2008) and Wiegand
(2004). When the best fit for the univariate
statistic has an error <0.025, the fit of the
parameter is acceptable, whereas an error >0.025
indicates an unacceptable fit. When the fit is not
acceptable, a complete spatial randomness (CSR)
null model is selected. For the bivariate statistic,
we postulated that taller tree height classes
suppress the recruitment and growth of lower
layers, but lower layers do not affect higher ones
(Nakashizuka 2001). Therefore, we fixed the
locations of the upper layer tree height class and
randomized the locations of the lower tree height
class using a Poisson cluster null model. Since a
662
larger ring width provides a smoother curve, we
chose a ring width of four.
For all the analyses, we used 499
randomizations in the null model of Monte Carlo
simulations to provide 99% confidence intervals
(Stoyan and Stoyan 1994). However, this approach
may not be used for testing observed pattern
against spatial model because a type I error may
occur when the value of O(r) is close to a
simulation envelop (Grabarnik et al. 2011;
Loosmore and Ford 2006). Therefore, we used a
goodness of fit (GoF) test to provide expected type
I error rates. Details of this procedure are provided
by Grabarnik et al. (2011) and Loosmore and Ford
(2006). We selected distance intervals of 0–50 m
when using GoF tests to assess departures from the
null model. We retained the results for further
analysis only when the observed p-value of the GoF
test was <0.01. The package ‘spatstat’ of R v. 2.14.0
software (R Core Development Team [2012]) was
applied to map the distribution of species, and
Programita software (2008) (Wiegand and
Moloney 2004) was used to compute the O-ring
statistics.
2 Results
2.1 Stand Structure
Table 1 presents the results of descriptive
statistics for species in the entire plot. Judging by
IVs, A. nephrolepis ranked as the most dominant,
with the highest values of number of individuals
(463) and basal area (12.726 m2/ ha). P. jezoensis
and Species of Acer ssp. were the second-most
dominant, with 154 individuals and 256 individuals,
respectively. Species of Betula ssp. was the fourth-
most dominant, and its value was 0.42. Although P.
koraiensis had only 94 individuals, it ranked the
fifth in terms of IV and exhibited the largest
maximum DBH (55.5 cm) among species. Tilia
amurensis had more trees than P. koraiensis (121
vs. 94 trees), and it ranked the sixth. These six tree
species accounted for 95% of the total IVs and were
therefore considered to be the dominant tree
species.
The observed diameter distribution of the six
dominant species is illustrated in Figure 1. All six
dominant species generally exhibited uneven-aged
 J. Mt. Sci.(2015) 12(3): 659-670

Figure 1 DBH class distributions of six dominant tree species in the 1-ha forest plot.

reversed J curves. The diameter distribution of

Table 2 Basic tree height characteristics of six
Picea species exhibited three peaks (at 5–10 cm, dominant species in two height classes: L,
20–25 cm, and 30–35 cm; Figure 1b). The same lower height class (h < 10 m); U, upper height
tendency was observed for Pinus, with three peaks class (h ≥ 10 m)
at 5–10 cm, 20–25 cm, and 35–40 cm (Figure 1c). Height (m) Number of trees
Species
According to the tree height data, among the Max Min Mean L U Total
Abies 21.9 4.1 11.5 164 299 463
basic quantity characteristics of the six dominant Picea 21.5 4.8 12.1 43 111 154
tree species at two height classes (Table 2), we Pinus 21.0 3.6 12.1 31 63 94
found that tree heights of Tilia, Betula and Acer Tilia 19.2 6.7 10.7 66 55 121
were no more than 20 m, with the tallest individual Betula 19.8 4.6 11.9 59 155 214
Acer 19.1 4.5 10.4 132 124 256
at 19.8 m. However, trees taller than 20 m were
Notes: Tilia = T. amurensis; Picea = P. jezoensis;
generally few in this mixed forest; Thus, we divided Pinus = P. koraiensis; Abies = A. nephrolepis; Betula
all species into two vertical layers: lower (L) and = Species group of Birch; Acer = Species group of
upper (U) representing trees of heights <10 m and Maple. (Similarly hereinafter)
≥10 m, respectively. In addition, members of
individual species considered as a whole (including For example, both Abies (A) and Abies (L)
both L and U) were represented by A. exhibited an aggregated distribution from 0 to 3 m
but a random or regular distribution at coarser
2.2 Spatial Patterns of Dominant Tree distances (Figure 3a, b). Abies (U) exhibited
Species in Different Vertical Layers random distributions at almost all distances
(Figure 3c), as did Picea (L) (Figure 3e). The two
Spatial distributions varied among the six categories of Picea (A and U) showed aggregated
dominant species at different vertical layers (Figure distributions at fine distances (<5 m), but as
2). As to all six dominant species distributed in the distance increased, random distributions were
plot, Pinus and Tilia were few in the center of the observed (Figure 3d, f). Pinus (A) was randomly
plot. The Picea and Pinus of lower height class distributed at the 0–1 m distance, whereas this
trees were fewer in the corner. Overall, rough species exhibited an aggregated distribution in 2–
visual observed in the figure, with an increment in 10 m, a regular distribution up to 35–39 m, and a
height class, the spatial distribution approached a random distribution at other distance intervals
random or regular distribution. (Figure 3g); Pinus (L) and Pinus (U) were
Spatial patterns of dominant tree species in randomly distributed at all distances (Figure 3h, i).
different vertical layers were illustrated in Figure 3. Trees of Tilia and Acer (A, L and U) had aggregated

663
J. Mt. Sci.(2015) 12(3): 659-670
Figure 2 The stem maps of dominant tree species at different height classes: ●: lower height class (height < 10 m);
□: upper height class (height ≥ 10 m).
distributions at fine distances, but as distance
between individuals increased, random and regular
distributions gradually appeared (Figure 3j–l and
3p–r). The two categories of Betula (A and L) were
random distributions at coarse distances. However,
Betula (U) showed aggregated distributions at the
4–13 m distance, and random distributions at
other distances (Figure 3m–o).Through the GoF
text, p-value of all six dominant species ranged
from 0.002 to 0.008 except trees of Pinus (L and
U), 0.028 and 0.098, respectively.
2.3 Intra- and Interspecies Spatial
Associations between Different Vertical
Layers
Intra- and interspecies spatial associations
between upper (U) and lower (L) tree height
classes varied with species, tree height, and
distance (Table 3). The GoF tests identified positive
associations for three species pairs: Tilia (U) –
Pinus (L) (0–8 m), Abies (U) – Abies (L) (0–9 m)
and Acer (U) – Acer (L) (0–9 m), and negative
associations for four species pairs: Pinus (U) –
Tilia (L) (1–7 m), Abies (U) – Tilia (L) (0–12 m),
Abies (U) – Acer (L) (1–13 m, and 15 m) and Picea
(U) – Tilia (L) (2–9 m). Additionally, Tilia (U) was
positively associated with Tilia (L) and Abies (L) at
664
distances of 0–2 m and 0–3 m, respectively.
Similarly, other four species pairs: Pinus (U) –
Pinus (L), Abies (U) – Pinus (L), Betula (U) –
Pinus (L) and Betula (U) – Betula (L) were
positively associated at fine distances, but as
distance increased, their relationships weakened
and became more independent. Picea (U) had a
negative association with Pinus (L) at distances of
7–10 m and 14–15 m, and a negative association
with Picea (L) at distance of 6–8 m, as did Abies (U)
– Betula (L) (0–1 m and 3 m) and Tilia (U) – Picea
(L) (2m and 7–8 m). There were no significant
relationships between Pinus (U) and Acer (L) or
between Abies (U) and Picea (L), or Acer (U) and
Picea (L) at almost distance intervals.
We also analyzed the spatial associations
among species within tree height classes (lower (L)
– lower (L) and upper (U) – upper (U)) (Figures 4
and 5). The category of species pairs: Pinus (L) –
Tilia (L) was positive association at a distance of
0–18 m (Figure 4f), and negative associations for
three species pairs: Picea (L) – Tilia (L) (0–9 m)
(Figure 4d). The other species pairs were spatial
independence at the most distances. Furthermore,
we observed spatial independence among other
species upper-tree-height class pairs at nearly all
distance intervals (Figure 5a–g). The p-values of
species within tree-height classes were calculated
from 0.002 to 0.008 in the GoF tests.
 J. Mt. Sci.(2015) 12(3): 659-670

Figure 3 Spatial patterns of six dominant tree species in different vertical layers. Black lines indicate ring statistics
(O11(r)); dashed lines indicate upper and lower limits of 99% confidence intervals. A: all types of an individual
species in one vertical layer; L: lower vertical layer; U: upper vertical layer. The p-values were calculated by
goodness-of-fit (GoF) tests. Only species pairs with p < 0.01 have been included.

uneven-aged mixed coniferous-broadleaf at its

3 Discussion early-successional stage of development. Most
frequency distributions of all six dominant species
The forest examined in the present study was tracked uneven-aged reversed J curves (Figure 1).

665
J. Mt. Sci.(2015) 12(3): 659-670

Table 3 Intra- and interspecies spatial associations of the lower vertical layer (L) to the upper
vertical layer (U)
Scale (m)
p-
Species 16- 35-
value 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
35 50
Tilia (U) - Tilia (L) 0.002 + + + r r r r r r r r r r r r r r r
Tilia (U) - Pinus (L) 0.002 + + r + + + + r + r r r r r r r r r(-)
Tilia (U) - Abies (L) 0.004 + + + r r r r r r r r r r r r r r r
Tilia (U) - Picea (L) 0.004 r r - r r r r - - r r r r r r r r r
Pinus (U) - Tilia (L) 0.002 r - - - - - - - r r r r r r r r r(-) r(+)
Pinus (U) - Pinus (L) 0.008 r r + + + + + r r r r r r r r r r r(-)
Pinus (U) - Acer (L) 0.002 r r r r r r r r r r r r r r r r r r
Abies (U) - Tilia (L) 0.002 - - - - - - - - - - - - - r r r r(+) r
Abies (U) - Pinus (L) 0.008 r r r r + + + r r r r r r r r r r r
Abies (U) - Abies (L) 0.002 + + + + + + + + r + r r r r r r r(-) r(+)
Abies (U) - Picea (L) 0.006 r r r r r r r r r r r r r r r r r r
Abies (U) - Betula (L) 0.006 - - r - r r r r r r r r r r r r r r
Abies (U) - Acer (L) 0.002 r - - - - - - - - - - - - - r - r(+) r(+)
Picea (U) - Tilia (L) 0.008 r r - r - r - - - - r r r r r r r(-) r(+)
Picea (U) - Pinus (L) 0.008 r r r r r r r - - - - r r r - - r r
Picea (U) - Picea (L) 0.002 r r r r r r - - - r r r r r r r r r
Betula (U) - Pinus (L) 0.004 r + + r + r r r r r r r r r r r r r
Betula (U) - Betula (L) 0.002 + + r r r r r r r r r r r r r r r r
Acer (U) - Picea (L) 0.008 r r + r r + r r r r r r r r r r r r
Acer (U) - Acer (L) 0.002 + + + + + + + + + + r r r r r r r r
Notes: +: positive association, -: negative association, r: no spatial association; + (r): more positive association
points than no associations; r (+): more no association points than positive associations; - (r): more negative
association points than no associations; r (-): more no association points than negative associations. The p-values
were calculated by goodness-of-fit (GoF) tests. Only species pairs with p < 0.01 have been included.

The frequency distributions of diameter for Picea
and Pinus species had three peaks. These may be
the reflection of adult tree losses to cyclone
“Bolaven”; dead standing trees belonged to diverse
diameter classes, which may account for the multi-
modal size class distributions. Trunk or branch
breakages under heavy snow loads may also have
influenced shapes of frequency distributions (Li et
al. 2004).
Forest spatial patterns are closely related to
distance (Cerrillo et al. 2013; Condit et al. 2000;
Yuan et al. 2011). Spatial distribution of trees may
fit one pattern at one interval and another at a
different interval (Schurr et al. 2004; Wiegand et al.
2000). We found that some tree species had
aggregated distributions at fine distances, but as
distances between individuals increased, random
or regular distributions occurred more frequently,
e.g., in the case of Abies (A) and (L), Picea (A) and
(U), Pinus (A), and Tilia and Acer. This pattern
possibly emerged due to lower height class
individuals required fewer resources. Moreover,
the aggregated distributions could also be
attributable to the limited seed dispersal ability of
these tree species, include the character of tree
seeds (e.g. the larger-sized pine cones of coniferous
tree species), or the seeds were obstructed by the
complex shape of breaches (Hubbell et al. 1999;
Seidler and Plotkin 2006; Tamme et al. 2010;
Zhang et al. 2011; Zou et al. 2007). Additionally,
environmental heterogeneity might also have been
contributed to the aggregated distributions of the
dominant trees at fine distances (Harms et al.
2000).
Random or regular distributions showed in
Abies and Pinus in the upper height class (Figure
3c, i). Similar results were obtained by previous
research (Hao et al. 2007; Miao et al. 2009). Adult
trees in the upper height class require more
resources, such as light, water, and nutrients, to
develop compared to juveniles (Boyden et al. 2005;
Druckenbrod et al. 2005; Quesada et al. 2009). The
limited resources available cannot meet the
demand for all trees; therefore, “self-thinning” is
likely triggered, causing the distribution to become
increasingly regular (Li 2010). Pinus (L) and Picea
(L) were mainly randomly distributed at the most
distances, the pattern that might be attributable to
human interference. For instance, pine cones were
collected for their economic value, and this activity

666
 J. Mt. Sci.(2015) 12(3): 659-670

Figure 4 Examples of intra- and inter-specific associations within tree height classes (lower (L)–lower (L)). Black
lines indicate ring statistics (O12(r)); dashed lines indicate upper and lower limits of 99% confidence intervals. The
p-values were calculated by goodness-of-fit (GoF) tests. Only species pairs with p < 0.01 have been included.

Figure 5 Examples of intra- and inter-specific associations

within tree height classes (upper (U)–upper (U)). Black
lines indicate ring statistics (O12(r)); dashed lines indicate
upper and lower limits of 99% confidence intervals. The p-
values were calculated by goodness-of-fit (GoF) tests. Only
species pairs with p < 0.01 have been included.

might account for the relative rarity of understory
Pinus trees (Liu et al. 2004; Tao et al. 1995).
The individuals of Pinus (L), Abies (L), and
Tilia (L) were positively associated with Tilia (U)
and Betula (U) at some distance intervals,
indicating that Pinus and Abies were able to thrive
under Tilia or Betula canopies as well as under
those that were conspecific. These findings
corroborate previous work (Zhang et al. 2007). In
addition, the lower height class coniferous species

667
J. Mt. Sci.(2015) 12(3): 659-670
and the upper broad-leaved species occupied
different ecological niche, which could utilize forest
resource more effective (Wang et al. 2011). There
were intra-specific positive associations between
trees in lower and upper height classes (e.g. Tilia,
Abies and Acer), suggesting that limited seed
dispersal from mother trees results in clusters of
small individuals within the seed rain shadows.
Thus, saplings recruit beneath the canopies of large
parent trees and must be shade-tolerant for long
term persistence (Hou et al. 2004; Zhao et al.
2012).
Lower height class broad-leaved species (Tilia,
Betula and Acer) were negatively associated with
other three coniferous species at coarse distances,
suggesting that canopies of some gymnosperms
provide unsuitable habitats for the recruitment of
Tilia (L), Betula (L) and Acer (L), presumably
through attenuation of incoming radiation. Zhang
et al. (2007) made similar observations. Therefore,
we conclude that different species have different
habitat requirements for persistence and
recruitment (Boyden et al. 2005; Harms et al.
2000), a premise that supports the regeneration
niche hypothesis (Grubb 1977). Picea (U) had
independent or negative associations with Picea (L)
and Pinus (L). Differential exclusion among Picea
height classes may relate to the unsuitability of
forest floor micro-environmental conditions for the
survival, establishment, and growth of juveniles
and sub-canopy trees. This is a finding that is to
some extent congruent with the Janzen-Connell
theory, which proposes high rates of mortality close
to mature trees (Wang et al. 2010; Zhao et al. 2012).
At most distances, there were no significant
associations between the following species pairs:
Tilia (U) and Picea (L), Abies (U) and Pinus (L),
Abies (U) and Picea (L), and Pinus (U) and Acer
(L).
Pinus (L) and Tilia (L) were positively
associated at most between tree distances, perhaps
because Pinus (L) and Tilia (U) occupy different
space, while Tilia saplings were sprouted tree
species on their mother trees. Therefore, we
recommend that Pinus (L) and Tilia (L) be
References
Allstadt A, Caraco T, Molnar F, et al. (2012) Interference
competition and invasion: Spatial structure, novel weapons
668
arranged together for artificial planting if necessary.
There were negative associations between Picea (L)
and Tilia (L) at the distance of 0–9 m, but they
were independent at other distances, perhaps
indicating spatial heterogeneity in distributions
between these two species in the lower canopy
(Hao et al. 2007; Zhang et al. 2010).
4 Conclusion
We explored the vertical spatial structure and
species associations among individuals of different
species at different height classes. This knowledge
can aid in efforts of forest management planning.
Saplings of coniferous tree species may be planted
with adult broad-leaved tree species possibly, such
as Pinus saplings and adult Tilia trees, as Pinus
saplings can grow and develop quite well under a
canopy of Tilia adults. However, due to the limited
experimental conditions, we did not include
saplings of DBH < 5 cm in our analysis. Therefore,
some discrepancies with previous studies may exist
in terms of spatial distribution patterns and spatial
associations within lower height classes (Hao et al.
2007; Zhang et al. 2007; Zhang et al. 2009). In
addition, the spatial patterns of species may have
been generated by the interplay of various factors,
such as selective cutting (Lei et al. 2007), forest fire
(Yu et al. 2009), physiological effects (Peres-Neto
and Legendre 2010), and disturbance (Allstadt et al.
2012). The assembly of long-term monitoring data
should be a priority for future studies.
Acknowledgements
This study was supported by the planning
projects of the introduction of international
advanced forestry science and technology in China
(948-project) (Grant No. 2013-4-66) and “The
Twelfth Five-Year-Plan” of National Science and
Technology for Rural Development in China (Grant
No. 2012BAD22B0203). The authors also thank
the editor and all anonymous reviewers for their
constructive suggestions.
and resistance zones. Journal of Theoretical Biology 306:46-
60. DOI: 10.1016/j.jtbi.2012.04.017

Boyden S, Binkley D, Shepperd W (2005) Spatial and temporal
patterns in structure, regeneration, and mortality of an old-
growth ponderosa pine forest in the Colorado Front Range.
Forest Ecology and Management 219(1):43-55. DOI:
10.1016/j.foreco.2005.08.041
Cerrillo RMN, Manzanedo RD, Bohorque J, et al. (2013)
Structure and spatio-temporal dynamics of cedar forests
along a management gradient in the Middle Atlas, Morocco.
Forest Ecology and Management 289: 341-353.
Chen J, Bradshaw GA (1999) Forest structure in space: a case
study of an old growth spruce-fir forest in Changbaishan
Natural Reserve, PR China. Forest Ecology and Management
120: 219-233.
Condit R, Ashton PS, Baker P, et al. (2000) Spatial patterns in
the distribution of tropical tree species. Science 288(5470):
1414-1418.
Dale MRT, Dixon P, Fortin MJ, et al. (2002) Conceptual and
mathematical relationships among methods for spatial
analysis. Ecography 25(5): 557-558.
Druckenbrod DL, Shugart HH, Davies I (2005) Spatial pattern
and process in forest stands within the Virginia piedmont.
Journal of Vegetation Science 16(1): 37-48. DOI: 10.1111/
j.1654-1103.2005.tb02336.x
Fajardo A, Goodburn JM, Graham J (2006) Spatial patterns of
regeneration in managed uneven-aged ponderosa pine
Douglas-fir forests of Western Montana, USA. Forest Ecology
and Management 223(1-3): 255-266.
Fortin MJ, Dale MRT (2005) Spatial Analysis [electronic
resource]: A Guide for Ecologists, Cambridge University Press.
p 100.
Gilbert GS (2002) Evolutionary ecology of plant diseases in
natural ecosystems. Annual Review of Phytopatholgy 40: 13-
43. DOI: 10.1146/annurev.phyto.40.021202.110417
Gong ZW, Kang XG, Gu L, et al. (2010) Spatial Pattern
Dynamics of Forest Succession in Spruce-fir Mixed Stand in
ChangbaiMountain, Northeast China. Journal of Northeast
Forestry University 38(1):44-46, 53. (In Chinese)
Grabarnik P, Myllymaki M, Stoyan D (2011) Correct testing of
mark independence for marked point patterns. Ecological
Modelling 222(23-24): 3888-3894. DOI: 10.1016/j.ecolmodel.
2011.10.005
Grubb PJ (1977) The maintenance of species-richness in plant
communities: the importance of the regeneration niche.
Biological Reviews 52(1): 107-145.
Hao ZQ, Zhang J, Song B, et al. (2007) Vertical structure and
spatial associations of dominant tree species in an old-growth
temperate forest. Forest Ecology and Management 252(1): 1-
11. DOI: 10.1016/j.foreco.2007.06.026
Harms KE, Wright SJ, Calderon O, et al. (2000) Pervasive
density-dependent recruitment enhances seedling diversity in
a tropical forest. Nature 404(6777): 493-495. DOI: 10.1038/
35006630
Hou JH, Mi XC, Liu CR, et al. (2004) Spatial patterns and
associations in a Quercus-Betula forest in northern China.
Journal of Vegetation Science 15(3): 407-414. DOI: 10.1111/
j.1654-1103.2004.tb02278.x
Hubbell SP, Foster RB, O'Brien ST, et al. (1999) Light-Gap
disturbances, recruitment limitation, and tree diversity in a
neotropical forest. Science 283(5401): 554-557.
Hui GY, Gadow KV (2003) Quantitative analysis of forest spatial
structure. China Science and Technology Press, Beijing, China.
pp 170-173. (In Chinese)
Larson AJ, Churchill D (2012) Tree spatial patterns in fire-
frequent forests of western North America, including
mechanisms of pattern formation and implications for
designing fuel reduction and restoration treatments. Forest
Ecology and Management 267: 74-92. DOI: 10.1016/j.foreco.
2011.11.038
Lei XD, Lu YC, Peng CH, et al. (2007) Growth and structure
development of semi-natural larch-spruce-fir (Larix olgensis-
Picea jezoensis-Abies nephrolepis) forests in northeast China:
12-year results after thinning. Forest Ecology and
J. Mt. Sci.(2015) 12(3): 659-670
Management 240(1): 165-177.
Li HD, Guan DX, Wang AZ, et al. (2013) Characteristics of
evaporation over broadleaved Korean pine forest in Changbai
Mountains, Northeast China during snow cover period in
winter. Chinese Journal of Applied Ecology 24(4): 1039-1046.
(In Chinese)
Li JQ (2010) Forest Ecology. Higher Education Press, 2nd ed,
Beijing. p 158. (In Chinese)
Li XF, Zhu JJ, Wang QL, et al. (2004) Snow/wind damage in
natural secondary forests in Liaodong mountainous regions of
Liaoning Province. Chinese Journal of Applied Ecology 15(6):
941-946. (In Chinese)
Liu ZG, Ji LZ, Hao ZQ, et al. (2004) Effect of cone-picking on
natural regeneration of Korean pine in Changbai Mountain
Nature Reserve. Chinese Journal of Applied Ecology 15(6):
958-962. (In Chinese)
Loosmore NB, Ford ED (2006) Statistical inference using the G
or K point pattern spatial statistics. Ecology 87(8): 1925-1931.
DOI: 10.1890/0012-9658(2006)87[1925:Siutgo]2.0.Co;2
Manabe T, Nishimura N, Miura M, et al. (2000) Population
structure and spatial patterns for trees in a temperate old-
growth evergreen broad-leaved forest in Japan. Plant Ecology
151(2): 181-197. DOI: 10.1023/A:1026512404110
Miao N, Liu SR, Shi HM, et al. (2009) Spatial patterns of
dominant tree species in sub-alpine Betula- Abies forest in
West Sichuan of China. Chinese Journal of Applied Ecology
20(6): 1262-1270. (In Chinese)
Nakashizuka T (2001) Species coexistence in temperate, mixed
deciduous forests. Trends in Ecology & Evolution 16(4): 205-
210.
Paluch JG (2007) The spatial pattern of a natural European
beech (Fagus sylvatica L.)-silver fir (Abies alba Mill.) forest:
A patch-mosaic perspective. Forest Ecology and Management
253(1): 161-170. DOI: 10.1016/j.foreco.2007.07.013
Peng CH (2000) Growth and yield models for uneven-aged
stands: past, present and future. Forest Ecology and
Management 132(2): 259-27.
Peres-Neto PR, Legendre P (2010) Estimating and controlling
for spatial structure in the study of ecological communities.
Global Ecology and Biogeography 19(2): 174-184. DOI:
10.1111/j.1466-8238.2009.00506.x
Perry GLW, Enright NJ, Miller BP, et al. (2008) Spatial patterns
in species-rich sclerophyll shrublands of southwestern
Australia. Journal of Vegetation Science 19(5): 705-716. DOI:
10.3170/2008-8-18441
Quesada M, Sanchez-Azofeifa GA, Alvarez-Anorve M, et al.
(2009) Succession and management of tropical dry forests in
the Americas: Review and new perspectives. Forest Ecology
and Management 258(6): 1014-1024.
Riginos C, Milton SJ, Wiegand T (2005) Context-dependent
interactions between adult shrubs and seedlings in a semi-
arid shrubland. Journal of Vegetation Science 16(3): 331-340.
Ripley BD (1981) Spatial Statistics. Hayward Wiley, New York,
USA. p 252.
Salas C, Lemay V, Nunez P, et al. (2006) Spatial patterns in an
old-growth Nothofagus obliqua forest in south-central Chile.
Forest Ecology and Management 231(1): 38-46.
Schurr FM, Bossdorf O, Milton SJ, et al. (2004) Spatial pattern
formation in semi-arid shrubland: a priori predicted versus
observed pattern characteristics. Plant Ecology 173(2): 271-
282. DOI: 10.1023/B:Vege.0000029335.13948.87
Seidler TG, Plotkin JB (2006) Seed dispersal and spatial pattern
in tropical trees. PLoS Biology 4(11): e344.
Shao GF, Schall P, Weishampel JF (1994) Dynamic simulations
of mixed broadleaved-Pinus koraiensis forests in the
Changbaishan biosphere reserve of China. Forest Ecology and
Management 70(1): 169-181.
Stone R (2006) Ecology - A threatened nature reserve breaks
down Asian borders. Science 313(5792): 1379-1380. DOI:
10.1126/science.313.5792.1379
Stoyan D, Penttinen A (2000) Recent applications of point
process methods in forestry statistics. Statistical Science 15(1):
669
J. Mt. Sci.(2015) 12(3): 659-670
61-78.
Stoyan D, Stoyan H (1994) Fractals, Random shapes and point
fields: methods of geometrical statistics. Wiley, Chichester. p
389.
Tamme R, Hiiesalu I, Laanisto L, et al. (2010) Environmental
heterogeneity, species diversity and co‐ existence at different
spatial scales. Journal of Vegetation Science 21(4): 796-801.
DOI: 10.1111/j.1654-1103.2010.01185.x
Tao DL, Zhao DC, Zhao SD, et al. (1995) Dependence of natural
regeneration of Korean Pine on animals-An out closure
experiment. Chinese Biodiversity 3(3):131-133. (In Chinese)
Wang CK (2006) Biomass allometric equations for 10 co-
occurring tree species in Chinese temperate forests. Forest
Ecology and Management 222(1): 9-16. DOI: 10.1016/
j.foreco.2005.10.074
Wang GL, Liu F (2011) The influence of gap creation on the
regeneration of Pinus tabuliformis planted forest and its role
in the near-natural cultivation strategy for planted forest
management. Forest Ecology and Management 262(3): 413-
423.
Wang XG (2010) Spatial distributions of species in an old-
growth temperate forest, northeastern China. Canadian
Journal of Forest Research 40 (6): 1011-1019. DOI: 10.1139/X
10-056
Wiegand K, Jeltsch F, Ward D (2000) Do spatial effects play a
role in the spatial distribution of desert-dwelling Acacia
raddiana. Journal of Vegetation Science 11(4): 473-484.
Wiegand T, Gunatilleke S, Gunatilleke N (2007a) Species
associations in a heterogeneous Sri lankan dipterocarp forest.
American Naturalist 170(4): E77-E95. DOI: 10.1086/521240
Wiegand T, Gunatilleke S, Gunatilleke N, et al. (2007b)
Analyzing the spatial structure of a Sri Lankan tree species
with multiple scales of clustering. Ecology 88(12): 3088-3102.
DOI: 10.1890/06-1350.1
Wiegand T, Moloney KA (2004) Rings, circles, and null-models
for point pattern analysis in ecology. Oikos 104(2): 209-229.
Xu XM, Harwood TD, Pautasso M, et al. (2009) Spatio-
temporal analysis of an invasive plant pathogen
(Phytophthora ramorum) in England and Wales. Ecography
670
32(3):504-516. DOI: 10.1111/j.1600-0587.2008.05597.x
Yu H, Wiegand T, Yang XH, et al. (2009) The impact of fire and
density-dependent mortality on the spatial patterns of a pine
forest in the Hulun Buir sandland, Inner Mongolia, China.
Forest Ecology and Management 257(10): 2098-2107.
Yuan ZQ, Gazol A, Wang XG, et al. (2011) Scale specific
determinants of tree diversity in an old growth temperate
forest in China. Basic and Applied Ecology 12(6): 488-495.
Zhang J, Hao ZQ, Song B, et al. (2007) Spatial distribution
patterns and associations of Pinus koraiensis and Tilia
amurensis in broad-leaved Korean pine mixed forest in
Changbai Mountains. Chinese Journal of Applied Ecology 18:
1681-1687. (In Chinese)
Zhang J, Hao ZQ, Sun IF, et al. (2009) Density dependence on
tree survival in an old-growth temperate forest in
northeastern China. Annals of Forest Science 66(2): 1-9. DOI:
10.1051/Forest/2008086
Zhang J, Song B, Li BH, et al. (2010) Spatial patterns and
associations of six congeneric species in an old-growth
temperate forest. Acta Oecologica 36(1): 29-38. DOI:
10.1016/j.actao.2009.09.005
Zhang JT (2004) Quantitative ecology. Science Press, Beijing.
pp 264-266. (In Chinese)
Zhang LW, Mi XC, Shao HB, et al. (2011) Strong plant-soil
associations in a heterogeneous subtropical broad-leaved
forest. Plant and soil 347(1-2): 211-220. DOI: 10.1007/s11104-
011-0839-2
Zhang MT, Kang XG, Cai S (2012) The models for growth
process of spruce-fir forest. The 2nd International Conference
on Computer Application and System Modeling (2012): 927-
931. DOI: 10.2991/iccasm.2012.236
Zhao HY, Kang XG, Guo ZQ, et al. (2012) Species Interactions in
Spruce-Fir Mixed Stands and Implications for Enrichment
Planting in the Changbai Mountains, China. Mountain
Research and Development 32(2): 187-196. DOI: 10.1659/
Mrd-Journal-D-11-00125.1
Zou L, Xie ZQ, Li QM, et al. (2007) Spatial and temporal pattern
of seed rain of Abies fargesii in Shennongjia Nature Reserve,
Hubei. Biodiversity Science 15(5): 500-509. (In Chinese)