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ORIGINAL PAPER
Seedling density dependence regulated by population density
and habitat filtering: Evidence from a mixed primary broad-leaved
Korean pine forest in Northeastern China
Jing Cao
1
&Chunyu Zhang
1
&Bo Zhao
1
&Xiaoyu Li
1
&Manman Hou
1
&Xiuhai Zhao
1
Received: 11 December 2017 / Accepted: 31 January 2018
#INRA and Springer-Verlag France SAS, part of Springer Nature 2018
Abstract
&Key message The effects of distance dependence, negative density dependence (NDD), phylogenetic density dependence,
and habitat filtering were integrated to provide additional evidence in temperate forest tree seedling survival. The main
focus of this study was to explore how population density and habitat filtering regulate NDD. An approach involving four
classes of population density and three classes of soil moisture was tested, including the effect of habitat variables to more
accurately evaluate the underlying ecological processes affecting the density dependence of seedlings.
&Context NDD is an important mechanism for the maintenance of species diversity across multiple life stages, particularly
during seedling recruitment. By regulating specific population structures to maintain species diversity, the effects of density
dependence and distance dependence are sometimes difficult to distinguish. Nevertheless, the contribution of NDD to commu-
nity assembly, relative to other processes such as habitat filtering, remains a subject of debate. Recently, it has been reported that
seedling survivals are also negatively correlated with phylogenetic relatedness between neighbors and focal individuals. This
effect is known as phylogenetic negative density dependence (PNDD). However, another opposite effect known as phylogenetic
positive density dependence (PPDD) has also been reported to exist.
&Aims The objectives of this study are to examine the following: (i) how population density affects negative density dependence
(NDD); (ii) how habitat filtering regulates the NDD; (iii) whether more evidence can be found for PNDD or PPDD and why; and
(iv) whether the intensity of negative density dependence is affected by the distance between parent trees and seedlings.
&Methods The study was conducted in a 20-ha primary mixed broad-leaved Korean pine forest in Changbai Mountain of China.
We used generalized linear mixed models to analyze how the seedling survival of 23 woody plant species relates to
Handling Editor: Aaron Weiskittel
Contribution of the co-authors
Jing Cao designed the experiment, ran the data analysis, and wrote the
paper, Chunyu Zhang designed the experiment and revised language, Bo
Zhao provide experimental ideas and assisted in calculating data, Xiaoyu
Li and Manman Hou carried out the experiment operation and
coordinated the data collection, and Xiuhai Zhao supervised the work
and coordinated the research project.
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s13595-018-0706-x) contains supplementary
material, which is available to authorized users.
*Xiuhai Zhao
zhaoxh@bjfu.edu.cn
Jing Cao
caojingsmart@163.com
Chunyu Zhang
zcy_0520@163.com
Bo Zhao
zhaobo2015@bjfu.edu.cn
Xiaoyu Li
leexiaoyu@hotmail.com
Manman Hou
710272546@qq.com
1
Research Center of Forest Management Engineering of State
Forestry Administration, Beijing Forestry University,
Beijing 100083, China
Annals of Forest Science (2018) 75:25
https://doi.org/10.1007/s13595-018-0706-x
neighborhoods and habitat variables. Four models were established with and without habitat variables, and two of the four
models were used to test how different population densities of focal seedlings and different gradients of habitat variable regulated
negative density dependence.
&Results The following results were obtained: (1) the strongest conspecific negative density dependence (CNDD) was found
within a radius of 15 m; (2) seedling survival were most strongly impacted by the density of conspecific seedling and adult
neighbors in habitats with relatively low soil moisture; (3) the effect of seedling-seedling CNDD was especially significant, when
densities ranged from 20 to 40 seedlings/4 m
2
, and (4) there were some evidences of phylogenetic positive density dependence
(PPDD), and the effect of seedling-seedling PPDD was increasing with an increase in soil moisture.
&Conclusion Our results demonstrate that conspecific negative density dependence played an important role in seedling survival,
which is closely related to habitat filtering and population density. However, we found some evidences of phylogenetic positive
density dependence. We suggest that future studies of neighborhood density dependence should increase awareness of evolu-
tionary relationships.
Keywords Conspecific negative density dependence (CNDD) .Habitat filtering .Phylogenetic density dependence .Population
density .Temp er at e fore st
1 Introduction
Negative density dependence (NDD) is regulating tree popu-
lations at every developmental stage from the seedling stage to
maturity (Harms et al. 2000;Peters2003;Wuetal.2016a).
Many previous studies, using seedlings, have attempted to
document NDD by examining the relationship of plant surviv-
al, recruitment or growth with the densities of conspecific
neighbors (Webb and Peart 2000;Chenetal.2010;Comita
et al. 2010; Johnson et al. 2012; Lin et al. 2012). Focal plants
were negatively as well as positively impacted by conspecific
and heterospecific neighbors, depending on local abiotic con-
ditions, microbial activity, insects, and other animals (Lebrija-
Trejos et al. 2014). Positive interactions found with
heterospecific neighbors might result from facilitation, specif-
ic responses to abiotic conditions and/or the so-called species
herd protection hypothesis (Comita and Hubbell 2009;Peters
2003; Lebrija-Trejos et al. 2014). Negative interactions with
conspecific neighbors might be caused by shared pests and/or
by competition for limiting resources (Lebrija-Trejos et al.
2014). A major mechanism, known as the Janzen-Connell
hypothesis, proposed that the maintenance of diversity is fa-
cilitated by a conspecific negative density dependence
(CNDD), whereby the proximity to adults of the same species
reduces seedling survival rates through attacks by host-
specific adversaries (Janzen 1970,1972). Furthermore, dis-
tance dependence, a basic part of the Janzen-Connell hypoth-
esis, has been extensively verified in tropical forests. Some
evidence of distance dependence effects were found in tem-
perate forests, and more evidence is required in order to to
expand the range of the verification.
Previously, negative density dependence was not consid-
ered as a universal biodiversity maintaining mechanism in
forest communities, because only a few abundant species
showed it (Hubbell 1979; Hubbell et al. 1990). However, later
studies found that negative density dependence was hidden by
limitations of survey methods, spatial heterogeneity, and nat-
ural disturbances (Zhu et al. 2009). Research methods gradu-
ally improved. When spatial heterogeneity was excluded, it
was found that population density was regulated by the effects
of negative density dependence (Hubbell et al. 1990; Wills
et al. 1997;Peters2003; Zhu et al. 2009).
Simply dividing the species into conspecific and
heterospecific species could hide the difference in the effect
of different species on a focal species (Pacala et al. 1996).
Recent studies have shown that phylogenetic relatedness of
neighbors is an important predictor of NDD, a pattern referred
to as phylogenetic density dependence (Webb et al. 2006;
Gonzalez et al. 2010; Metz et al. 2010; Ness et al. 2011).
This pattern is consistent with the observation that herbivo-
rous insects are frequently associated with clades of host
plants (Novotny et al. 2010) and that pathogenic transmission
between pairs of tree species is more likely to occur if the
species are phylogenetically related (Gilbert and Webb
2007). The indices of phylogenetic dissimilarity (Wu et al.
2016a), as well as phylogenetically correlated plant traits
(Coley and Barone 1996), are accepted to be applications of
the phylogenetic approach. However, the results of phyloge-
netic density dependence vary. Several previous studies have
provided some evidence to support phylogenetic negative
density dependence (PNDD; Bagchi et al. 2010;Metzetal.
2010; Paine et al. 2012). In addition, some studies have iden-
tified phylogenetic positive density dependence (PPDD;
Lebrija-Trejos et al. 2014; Zhu et al. 2015;Wuetal.2016a).
Therefore, a large amount of evidence is required to confirm
the existence of phylogenetic density dependence.
Both in theoretical models and in experiments, it has been
shown that negative density dependence (NDD) could reduce
25 Page 2 of 12 Annals of Forest Science (2018) 75:25
interspecific competition exclusion and improve species di-
versity (Harms et al. 2000). Most field experiments did not
consider the disturbance caused by other factors such as hab-
itat heterogeneity which may affect the accuracy of the model
parameters (Clark et al. 1998; Dieckmann et al. 1999;Condit
et al. 2000; but see Zhu et al. 2009). Detecting NDD effects
may therefore be difficult (He and Duncan 2000;Wright
2002; Getzin et al. 2008). Some studies divided the habitat
into different types to examine habitat preferences of certain
species by analyzing the association between species occur-
rence and certain habitat variables, like topography, radiation,
and availability of soil nutrients and water, at the seedling
stage (Webb and Peart 2000; Comita et al. 2007;Johnetal.
2007; Comita and Engelbrecht 2009;Metz2012). It is thus
likely that habitat preferences and NDD operate simultaneous-
ly to produce the observed species composition and resulting
population dynamics (Comita et al. 2009;Chenetal.2010;
Bai et al. 2012;Piaoetal.2013). In order to verify such a
scenario, nested models, which consider the effects of density,
with and without an abiotic context, are required. Therefore, it
would be of interest to know how habitat filtering regulates
conspecific and phylogenetic density dependence.
The purpose of this study is to explore the effect of popu-
lation density on population structure and the influence of
different environmental gradients on negative density depen-
dence (NDD). The specific questions which we strive to an-
swer are the following: (i) How does population density affect
the NDD? (ii) How does habitat filtering regulate the NDD?
(iii) Can additional evidence be found for phylogenetic nega-
tive density dependence (PNDD) or phylogenetic positive
density dependence (PPDD) and why? (iv) Is the intensity of
negative density dependence affected by the distance between
parent trees and seedlings?
2Methods
2.1 Study site and seedling quadrates
Our study was conducted within a 20-ha mixed dynamic primary
broad-leaved Korean pine forest plot (BKP) (Fig. 1a, b), located
at the Changbai Mountain in Jilin Province, northeastern China
(42° 20′N, 127° 54′E). The elevation of the study area ranges
from 975 to 997 m (Fig. 1c). The area is characterized by a
temperate continental climate, with cold windy winters and wet
summers. The mean annual temperature is 2.9 °C, and precipita-
tion amounts are 600 to 900 mm. The soil is classified as a dark
brown forest soil (Wu et al. 2016b). The BKP plot (400 × 500 m)
was established in 2014. All of the woody stems with diameters
at breast height (DBH) ≥1 cm were tagged, identified, measured,
and mapped (see detailed methods in Condit 1998). The domi-
nant tree species are Korean pine (Pinus koraiensis Sieb. et
Zucc.), Amur linden (Tilia amurensis Rupr.), Manchurian ash
(Fraxinus mandschurica Rupr.), Mongolian oak (Quercus
mongolica Fisch. ex Ledeb.), and Mono maple (Acer mono
Maxim.). The basal area of our mixed primary broad-leaved
Korean pine forest stand was 42.82 m
2
/ha.
From May to August 2016, a total of 130 seedling quad-
rates (2 m × 2 m, 4 m
2
) were established in a regular pattern
within the center of each 40 m × 40 m subplot in BKP plot
(Fig. 1d). Where obstacles such as streams, large trees, rocks
or fallen trees prevented the establishment of a seedling quad-
rate, we placed it instead in a nearby 5-m × 5-m subplots. In
each of the 130 seedling quadrates, all of the woody plants
(trees, shrubs and lianas) as well as seedlings with DBH <
1 cm were tagged, identified by species, and measured for
height. In this study, all seedlings with DBH < 1 cm were used
as focal seedlings, because what we want to explore is the
density dependence of the whole seedling stage. Seedling
quadrats were censused once a month through the whole
growing season (from May to August), a total of four times.
In each census, the states (alive or dead) of all the woody
seedlings alive at the previous census were recorded and all
new recruits were identified and tagged.
2.2 Neighborhood variables
We defined the total seedling neighbor density of each seed-
ling quadrate as the number of seedlings within the quadrate.
The conspecific and heterospecific seedling neighbor densi-
ties were defined similarly. The seedlings which were impos-
sible to classify by species were included in the heterospecific
neighbor counts, but not as the focal seedlings. The total adult
neighbor density (TA) was calculated as the summed basal
area (BA) of the nearby adults weighted by their distances to
the focal seedling (Canham et al. 2004)asfollows:
TA ¼∑
N
i
BAi
Distancei
where Nis the number of adult neighbors. The conspecific and
heterospecific adult neighbor densities were calculated in the
same way. The density models were calculated over distances
of 5, 10, 15, and 20 m, in order to discuss which had the
stronger support. All our seedling quadrates were within
40 m of the edge of the BKP plot and therefore had incomplete
adult neighbor density values.
2.3 Construction of phylogenetic trees and indices
of phylogenetic dissimilarity
Four phylogenetic diversity indices were used to quantify
phylogenetic dissimilarities between the focal seedlings and
their heterospecific neighbors in our analyses. The indices
included total phylogenetic diversity (TOTPd), average phy-
logenetic diversity (AVEPd), relative average phylogenetic
Annals of Forest Science (2018) 75:25 Page 3 of 12 25
25 Page 4 of 12 Annals of Forest Science (2018) 75:25
diversity (APd′) and relative nearest taxon phylogenetic diver-
sity (NTPd′). A phylogenetic tree was built for adult trees, as
well as for the seedling species occurring in the plot, using a
Phylomatic program (Webb and Donoghue 2005)basedon
APGIII (Angiosperm Phylogeny Group 2009). Using this tree
algorithm, the four phylogenetic diversity indices were sepa-
rately calculated, from the focal seedlings to all the other
heterospecific seedlings within the plot, as well as the
heterospecific adult neighbors within each of the 5, 10, 15,
and 20 m radial plots. We recalculated the four phylogenetic
diversity indices; as a result, the models with densities calcu-
lated APd indices had stronger support than those indices with
densities otherwise calculated. The sAPd′and aAPd′represent
for phylodiversity between the focal seedling and the
heterospecific seedling neighbors and adult neighbors,
respectively.
2.4 Habitat variables
The habitat variables for each of the 130 target seedling quad-
rates were characterized using the following measurements:
canopy openness (light), soil moisture (SM), pH, litter thick-
ness (LT), and herbal density (HD). The BKP plot is relatively
flat and has no special topography such as ditches, ridges and
valleys, so the effect of topography on seedling survival was
not considered in this study.
Canopy openness For each seedling quadrat, we used hemi-
spherical photographs to measured canopy openness, it indi-
cated the light condition in the understory. Hemispherical pho-
tographs were taken 1.3 m aboveground at the center of each
quadrat, using a Nikon Coolpix 4500 camera equipped with a
Nikon FC-E8 Fisheye Converter lens (Tokyo, Japan) in
January 2014. For each quadrat, photographs were taken in
uniformly overcast weather once a mouth. The photograph
showing the highest contrast between sky and foliage for each
quadrat was selected. Digital Plant Canopy Imager CI-
110(China) was used to process photos and to calculate the
light transmittance.
Soil moisture For each seedling quadrat, we used a HH2
Moisture Meter (made in the UK) to measure soil moisture
once a mouth. By inserting the probe into the soil, instanta-
neous soil moisture data were obtained. Average values were
used for each quadrat.
pH We randomly chose two soil samples (500 g) which were
taken from surface layers (0–20 cm) in each seedling quadrat
and analyzed the samples at the laboratory. The Precision pH
Meter Tester PHS-25 (made in China) was used to determine
the soil pH value. The mean of the two samples was taken as
the final value of each quadrat measurement.
Measuring effects of litter thickness Surface litter intercepted
and captured a large amount of rainwater, thus increasing soil
moisture which effectively inhibited forest soil water evapo-
ration and forest soil moisture. The effects of different litter
thickness on soil moisture were assessed. We selected three
random points in each seedling quadrat to measure litter
thickness.
Herbal density Two herb quadrats (1 m × 1 m) were placed on
the side of each seedling quadrat (Fig. 1d); all the herbaceous
plants were tagged, identified by species and measured for
abundance. Each quadrat was surveyed once a month.
2.5 Statistical analysis
The seedlings individual survival (lived/died) from May to
August 2016 was modeled as a logistic function of the neigh-
borhood densities, habitat variables, and phylogenetic related-
ness using generalized linear mixed models (GLMMs) ap-
plied in the lme4 package in R 3.0.2. To exclude spatial
auto-correlation caused by some unexplored factors (Wu
et al. 2016a), we added tree seedling species and quadrats as
random effects our models in our study. The focal seedling
height was log-transformed, and all continuous explanatory
variables were standardized before analyses. Four models
(Table 1) were established to explore the effect of habitat
filtering on the detection of CNDD and PNDD, following
the method applied by Paine et al. (2012)andWuetal.
(2016a). The four models are presented in Table 1:a
density-dependent model (model I), a density + habitat model
with the same neighborhood variables as those in the density-
dependent model (model II), a phylogenetic density depen-
dent model (model III), and a phylogenetic + habitat model
with the same neighborhood variables as those in the phylo-
genetic density-dependent model (model IV). Akaike’sinfor-
mation criterion (AIC) was used to compare models.
3 Results
3.1 Distance dependence for seedling survival
in the best-fitting model
The density + habitat model (model II) and the phylogenetic +
habitat model (model IV) were found to indicate stronger neg-
ative density effects than the other models (without habitat
variables) at the 15-m radial scale (Table 2; Fig. 2). We did
not observe any significant interactions between the
Fig. 1 The spatial distribution in 20-ha mixed dynamic primary broad-
leaved Korean pine forest plot (BKP) in northeastern China. aMap of
China showing location of the study area. bA topographic map of BKP
plot. cContour map of BKP plot. dThe layout of seedling quadrats in
BKP plot
R
Annals of Forest Science (2018) 75:25 Page 5 of 12 25
probability of seedling survival and habitat variables and the
seedling-seedling densities or the phylogenetic neighbor den-
sities. Therefore, we assume that there is a density threshold in
the density dependence. Models II and IV with a 15-m radius
were chosen to verify whether seedling survival rates were
affected by both neighboring seedlings and adult neighbors.
Simultaneously, we explored whether or not phylogenetic
density played a key role in the survival rates of seedlings.
3.2 Density dependence affects by population density
The observed densities of the focal seedlings per 4 m
2
(D4)
were divided into four classes (less than 20 seedlings/4 m
2
;
20 ≤D4 < 30 seedlings/4 m
2
;30≤D4< 40 seedlings/4 m
2
;
D4 ≥40 seedlings/4 m
2
). Two models (II and IV) were
established with these four units. The results show an increas-
ing trend of significant seedling-seedling conspecific negative
density dependence (CNDD) with rising of threshold
(Table 3).The effect of seedling-seedling CNDD was especial-
ly significant, when densities were ranged from 20 to 40 seed-
lings/4 m
2
. Conspecific adult neighbor densities had a signif-
icantly negative impact on seedling survival only when the
density threshold < 20 seedlings/4 m
2
(Table 3). When density
threshold was between 30 and 40 seedlings/4 m
2
, seedling
survival rates were significantly positively impacted by
heterospecific adult neighbors in model II (Table 3). We found
negative effects of phylogenetic seedling-seedling diversity,
indicating that increased phylogenetic similarities between
heterospecific neighbors and focal seedlings caused an in-
crease in seedling survival (Table 3). Seedling survival rates
were significantly and positively impacted by the phylogenet-
ic relatedness of seedling neighbors but were negatively af-
fected by the phylogenetic relatedness of adult neighbors
(Table 3). Seedlings surrounded by more closely related seed-
ling neighbors had a higher probability of survival. Both
seedling-seedling and seedling-adult phylogenetic density de-
pendence were discovered when the focal seeding density<
20 seedlings/4 m
2
(Table 3). Across all units, seedling survival
rates were significant positively impacted by soil moisture.
The population density of all 23 species was at least
30 seedlings/4 m
2
in the study area. Fifteen of the 23 species
had a density of 30 to 40 seedlings/4 m
2
. Only 4 of the 23
species had a density higher than 40 seedlings/4 m
2
.The
species-level effects of conspecific seedling survival rates
were negative for adult neighbors in 91% of the species and
for seedling neighbors in 13% of species when the population
density ≤20 seedlings/4 m
2
(Fig. 3a, e). A population densi-
ty> 20 and ≤30 seedlings/4 m
2
also had a significant effect on
seedling survival for adult neighbors in 13% and for seedling
neighbors in 56% of species (Fig. 3b, f). A population densi-
ty> 30 and ≤40 seedlings/4 m
2
also had a significant effect on
seedling survival for adult neighbors in 20% and for seedling
neighbors in 93% of all species (Fig. 3c, g). Finally, a popu-
lation density> 40 seedlings/4 m
2
had no significant effect on
either adult or seedling neighbors (Fig. 3d, h). Seedling sur-
vival rates decreased for most species with increasing conspe-
cific population density.
3.3 How does habitat filtering regulate density
dependence
As can be seen in Table 3, the seedling survival was affected
by different habitat variables, and the strengths of these effects
were different. We propose that habitat filtering will result in
different effects of density dependence by controlling the hab-
itat conditions. Soil moisture was highly correlated with
Table 1 Description of the four models
Model Form Purpose
Model I Density-dependent model Ss = Cons + Hets + CA+ HA +
(1|quadrat)
Rxandom
+ (1|species)
Random
To assess the role of neighbor densities on
seedling survival
Model II Density + habitat model Ss = Cons + Hets + CA+ HA + SM
+ Ph + LT + Light + HD + (1|quadrat)
Random
+ (1|species)
Random
To explore the influence of habitat
filtering on the detection of CNDD
Model III Phylogenetic density dependent
model
Ss = Cons + CA + sAVd′+aAVd′
+ (1|quadrat)
Random
+ (1|species)
Random
To assess the importance of evolutionary
relationships in the survival model
Model IV Phylogenetic density dependent +
habitat model
Ss = Cons + CA + sAVd′+aAVd′
+ SM + Ph + LT + Light + HD
+ (1|quadrat)
Random
+ (1|species)
Random
To explore the influence of habitat
filtering on the detection of PNDD
Neighborhood variables included the density of conspecific seedling neighbors (Cons), the density of heterospecific seedling neighbors (Hets), sum of
conspecific adults’basal areas weighted by the distance between the focal seedling and the adult neighbors (CA), sum of heterospecific adults’basal
areas weighted by the distance between the focal seedling and the adult neighbors (HA), and two phylogenetic diversity indices: relative average
phylogenetic diversity between heterospecific seedling neighbors and focal seedlings (sAVd′) and relative average phylogenetic diversity between
heterospecific adult neighbors and focal seedlings (aAVd′). Habitat variables included the percentage of canopy openness (light), soil moisture (SM),
pH, litter thickness (LT), and herbal density (HD)
Ss seedling survival
25 Page 6 of 12 Annals of Forest Science (2018) 75:25
survival in each density threshold unit with each model
(Table 3). Therefore, we used soil moisture conditions
as an example to verify the proposed hypothesis
(Table 4). The median value of the soil moisture was
45%. Therefore, we divided the soil moisture variable
into three gradients (soil moisture ≤42, 45, and 48%)
to establish the models. Seedling survival rates were
significantly negatively affected by conspecific seedling
neighbors when soil moisture ≤42 or ≤45%.
Conspecific adult neighbor densities had a significant
negative impact on seedling survival only when soil
moisture ≤42% (Table 4). Both heterospecific adult
neighbor densities and heterospecific adult neighbor
densities positively affected seedling survival when soil
moisture ≤45%. Seedling survival rates were positively
impacted by phylogenetic relatedness of seedling
neighbors in each unit and positively affected by phy-
logenetic relatedness of adult neighbors when soil
moisture ≤48% (Table 4). It seems that the intensity
of radiation on seedling survival was enhanced with
decreasing soil moisture thresholds (Table 4). Soil
moisture was low where radiation was strong in micro-
habitats, and the survival limitation caused by soil
moisture was reduced. We also found that seedling
survival was only significantly and negatively correlat-
ed with litter thicknesses (LT) in one case (soil mois-
ture ≤48%) (Table 4). We concluded that if the LT
layer is thicker, it will prevent the rainwater to reach
the soil. As a result, both the soil moisture and conse-
quently the probability of seedling survival will be
-0.4 -0.3 -0.2 -0.1 0.0 0.1 0.2
-0.4 -0. 3 -0.2 -0.1 0.0 0.1 0.2
density dependent
model
-0.4 -0.3 -0.2 -0.1 0.0 0.1 0.2
5m radius
10m radius
15m radius
20m radius
Effect of cons
p
ecific adult densit
y
-0.4 -0.3 -0. 2 -0.1 0. 0 0.1 0.2
phylogenetic
density dependent
model
5m radius
10m radius
15m radius
20m radius density dependent
+ habitat model
Effect of cons
p
ecific adult densit
y
phylogenetic
density dependent
+ habitat model
Fig. 2 Neighborhood effects of
conspecific adult neighbor
density on seedling survival at
scales of 5, 10, 15, and 20 m with
four models (models I, II, III, IV).
aDensity-dependent model
(model I). bDensity + habitat
model (model II). cPhylogenetic
density-dependent model (model
III). dPhylogenetic + habitat
model. Estimated coefficients (±
SE) from models are shown
separately for four scales. The
black circles indicate significant
effects (P< 0.05), gray circles
signify marginally significant
effects (0.05 < P< 0.1), and white
circles mean no significance.
Double negative signs: significant
negative effects, single negative
sign: signify marginally
significant negative effects
Table 2 The AIC and BIC values for the comparison of four models at scales of 5, 10, 15, and 20 m
Model AIC BIC
5 m radial
scale
10 m radial
scale
15 m radial
scale
20 m radial
scale
5mradial
scale
10 m radial
scale
15 m radial
scale
20 m radial
scale
Model I 869.0 874.4 826.7 873.4 903.5 903.5 861.7 892.0
Model II 866.3 869.0 827.7 829.7 884.9 893.1 846.0 861.7
Model III 861.2 874.6 829.0 866.2 895.6 903.2 861.8 884.8
Model
IV
859.1 868.6 827.8 829.6 877.6 893.3 846.3 861.8
Annals of Forest Science (2018) 75:25 Page 7 of 12 25
Table 3 Coefficient estimates for all explanatory variables in the density + habitat model (model II) and the phylogenetic + habitat model (model IV)
with four classes of focal seedling population density
Explanatory variables D4 < 20 (seedlings/4 m
2
)20≤D4 < 30 (seedlings/4 m
2
)30≤D4 < 40 (seedlings/4 m
2
)D4≥40 (seedlings/4 m
2
)
Model II Model IV Model II Model IV Model II Model IV Model II Model IV
Cons −0.17 −0.26* −0.21 −0.27** −0.31** −0.33** −0.21 0.22
Hets 0.19 0.03 0.05 0.13
CA −0.30* −0.25* 0.06 −0.02 0.07 −0.02 0.02 0.03
HA 0.05 0.19 0.18* 0.21
sAVd’−0.14 −0.21* −0.16* −0.24**
aAVd’0.11 0.27** 0.14 0.15
SM 0.26** 0.25** 0.33** 0.28** 0.40*** 0.30** 0.44*** 0.22
Ph −0.06 −0.04 −0.05 −0.02 −0.32*** −0.26** −0.43** 0.20
LT −0.08 −0.12 −0.14 −0.27*** −0.38*** −0.45*** −0.45*** 0.14***
Light −0.09 −0.11 −0.09 −0.16* 0.13. 0.06 0.24 0.14
HD 0.32* 0.35** 0.03 0.05 0.70*** 0.70*** 1.07** 0.87
AIC 304.5 294.1 216.3 205.4 162.8 152.2 135.2 119.1
No asterisk, not significant. Neighborhoodvariables included the density of conspecific seedling neighbors (Cons), the density of heterospecificseedling
neighbors (Hets), sum of conspecific adults’basal areas weighted by the distance between the focal seedling and the adult neighbors (CA), sum of
heterospecific adults’basal areas weighted by the distance between the focal seedling and the adult neighbors (HA), and two phylogenetic diversity
indices: relative average phylogenetic diversity between heterospecific seedling neighbors andfocal seedlings (sAVd′) and relative average phylogenetic
diversity between heterospecific adult neighbors and focal seedlings (aAVd′). Habitat variables included the percentage of canopy openness (light), soil
moisture (SM), pH, litter thickness (LT), and herbal density (HD)
*P<0.05;**P< 0.01; ***P<0.001
-0.3 -0.2 -0.1 0.0 0.1
Numbers of species
0
2
4
6
8
10
-0.3 -0.2 -0.1 0.0 0.1
-0.3 -0.2 -0.1 0.0 0.1
-0.3 -0.2 -0.1 0.0 0.1
-0.3 -0.2 -0.1 0.0 0.1
0
2
4
6
8
10
-0.3 -0.2 -0.1 0.0 0.1
-0.3 -0.2 -0.1 0.0 0.1
-0.3 -0.2 -0.1 0.0 0.1
Effect of conspecific adult neighbors
Effect of conspecific seedlin
g
nei
g
hbors
ab c d
ef gh
Fig. 3 Histograms showing Pvalues (x-axis) of conspecific seedling and
adult neighbor densities on survival for 23 tree species in the Changbai
Mountain 20-ha forest dynamics plot. For seedlings, two types of
neighbors were analyzed as follows: seedlings and adults. Dashed lines
are at zero, so that bars to the left of the line indicate a negative effect of
the neighborhood variable on survival, while bars to the right indicate a
positive effect on survival. a,eD4 < 20 seedlings/4 m
2
.b,f20 ≤D4 <
30 seedlings/4 m
2
.c,g30 ≤D4 < 40 seedlings/4 m
2
.d,hD4 >
40 seedlings/4 m
2
25 Page 8 of 12 Annals of Forest Science (2018) 75:25
affected. Seedling survival was significantly and posi-
tively affected by herbal density, an important habitat
variable (Table 4). This result was not expected.
4 Discussion
In this study, we used a data set of 3268 seedlings
including 23 woody plant species in a 20-ha primary
broad-leaved Korean pine forest plot, located in the
Changbai Mountain area of northeastern China. We ex-
plored the relative importance of conspecific negative
density dependence (CNDD) and phylogenetic density
dependence which affected by habitat filtering and pop-
ulation density in seedling survival using generalized
linear mixed models (GLMMs). The models were built
for seedlings which depend for their survival on the
densities of conspecific and heterospecific neighbors,
considering the phylogenetic dissimilarities between
the heterospecific neighbors and the focal seedlings.
Each of these models was developed with and without
habitat variables, in order to determine the degree to
which habitat filtering affected the apparent prevalence
of NDD. We analyze the distance effect with each mod-
el to explore the influence of distance on density depen-
dence. In particular, models were built with added
thresholds of population density and habitat variable
gradients.
4.1 The effects of distance on density dependence
The effects of density dependence and distance dependence
on plant populations are both important. Distance dependence
is the most fundamental part of the Janzen-Connell hypothesis
and widely verified (Hubbell and Foster 1983; Wright 2002).
Connell (1971) found a strong dependence effect on seedling
survival and parent tree distance. Hyatt et al. (2003) found
greater distance dependence effects in seedlings than in seeds.
Wright (2002) and Petermann et al. (2008)reportedthatthe
effects of distance dependence on community dynamics were
underestimated in most studies including BCI plots. There are
many reasons why the universality of distance-dependent ef-
fects in plant communities is underestimated, one of the rea-
sons being seed dispersal limitation. Seeds usually fall close to
the parent trees, and the seedlings are mostly gathered near
their parent trees. If we just analyzed neighboring individual
numbers, we might underestimate the effect of distance de-
pendence. Therefore, we calculated the total adult neighbor
density (TA) as the summed basal area (BA) of the nearby
adults weighted by their distances to the focal seedling. Four
radial scales with distances from the adult neighbors to the
seedling quadrates of 5, 10, 15, and 20 m were used.
Table 4 Coefficient estimates for
all explanatory variables in the
density + habitat model (model II)
and the phylogenetic + habitat
model (model IV) with three
classes of soil moisture
Explanatory variables Soil moisture ≤42% Soil moisture ≤45% Soil moisture ≤48%
Model II Model IV Model II Model IV Model II Model IV
Cons −0.48*** −0.50*** −0.47*** −0.41*** −0.25 −0.22
Hets −0.03 0.14* −0.01
CA 0.01 −0.12 0.06 −0.05 0.09 0.00
HA 0.10 0.15* 0.16
sAVd′−0.10 −0.12* −0.18*
aAVd′−0.07 −0.05 0.24*
SM 0.08 0.02 0.16* 0.09 0.13 0.19
Ph −0.21** −0.19* −0.33*** −0.31*** −0.09 −0.03
LT 0.04 0.04 0.02 −0.04 −0.05 −0.24**
Light −0.15* −0.26** −0.11* −0.19* −0.11 −0.12
HD 0.24 0.24 0.31** 0.34** −0.01 0.10
AIC 128.1 117.2 156.2 150.2 209.1 196.1
No asterisk, not significant. Neighborhood variables included the density of conspecific seedling neighbors
(Cons), the density of heterospecific seedling neighbors (Hets), sum of conspecific adults’basal areas weighted
by the distance between the focal seedling and the adult neighbors (CA), sum of heterospecific adults’basal areas
weighted by the distance between the focal seedling and the adult neighbors (HA), and two phylogenetic diversity
indices: relative average phylogenetic diversity between heterospecific seedling neighbors and focal seedlings
(sAVd′) and relative average phylogenetic diversity between heterospecific adult neighbors and focal seedlings
(aAVd′). Habitat variables included the percentage of canopy openness (light), soil moisture (SM), pH, litter
thickness (LT), and herbal density (HD)
*P<0
.05; **P<0.01; ***P<0.001
Annals of Forest Science (2018) 75:25 Page 9 of 12 25
In this study, we analyzed the relationships between seed-
ling survival rates, environmental factors, phylogenetic relat-
edness, seedling neighbor densities, and adult neighbor den-
sities within these four radii (5, 10, 15, and 20 m). The models
with densities calculated over a distance of 15 m were found to
have the strongest effect. The effect of distance on density
dependence was very strong. Wu et al. (2016a) found that a
distance of less than 20 m had strong effects when they studied
density dependence within a tropical forest in Xishuangbanna
China.
4.2 The evidence of PNDD and PPDD
Several studies have focused on the effect of heterospecific
neighbors on negative density dependence based on phyloge-
netic relatedness (Metz et al. 2010; Paine et al. 2012). For
example, Liu et al. (2012) evaluated the phylogenetic
Janzen-Connell effect, which may be caused by associated
host-specific fungal pathogens in subtropical forests. In our
results, we found evidence of phylogenetic negative density
dependence (PNDD) in agreement with the studies of Metz
et al. (2010) who found that seedling survival rates increased
in cases where nearby adult neighbors were more distantly
related to the focal seedlings. The critical factors affecting
pathogen infection of a host plant are known to be morpho-
logical and biochemical, which are often phylogenetically
conserved (Mitter et al. 1991). There is much empirical evi-
dence that closely related species which also have several
similar key functional traits are more likely to share the same
or similar pests and pathogens (Novotny et al. 2006;Gilbert
and Webb 2007; Gilbert et al. 2012; Liu et al. 2012;Yangetal.
2014). Therefore, the effects of neighbors on a focal plant
should be dependent on their phylogenetic similarities and
should be less negative for plants which are less related.
However, Wu et al. (2016a) found that seedling survival rates
were higher among closely related heterospecific neighbors
and considered the possibility that unobserved habitat factors
may have confounding effects, although it was not very clear
what these factors might be. However, there was evidence of
phylogenetic positive density dependence (PPDD). Our re-
sults were in line with the findings of Wu et al. (2016a,b)in
the Xi Shuang Ban Na tropical forest and consistent with the
studies of Lebrija-Trejos et al. (2014)andZhuetal.(2015)in
the Barro Colorado (BCI) plot. Especially, Lebrija-Trejos et al.
(2014) found a positive relationship between first-year seed-
ling survival and the proportion of closely related
heterospecific neighbors in the BCI plot. In our study, all of
the woody plants as well as seedlings with DBH < 1 cm were
tagged; earlier seedling stages were explored in models, in-
cluding the first-year seedlings. The strength of the effect of
seedling-seedling PPDD increased with higher soil moisture
(Table 4). Such evidence is likely the result of closely related
species sharing similar habitat resources (Zhu et al. 2015).
4.3 The effects of the population density on density
dependence
Conspecific seedling-seedling and seedling-adult negative
density dependence (CNDD) have been reported many times
in tropical and subtropical as well as temperate forests
(Johnson et al. 2012,Piaoetal.2013, Zhu et al. 2015;Wu
et al. 2016a,b). In less dense patches (population density <
20), both conspecific adult and seedling neighbor densities
had significant negative impact on seedling survival. A possi-
ble explanation is that there may be many more conspecific
seedling neighbors around their presence over the wider area
(beyond our seedling quadrats) (Wu et al. 2016a). The impact
of conspecific neighbors on survival appears to be substantial-
ly larger with high population density; such relationships may
be involved in intraspecific competition for shared resources.
Meanwhile, clustering of conspecific individuals may attract
more natural special pests and pathogens (Janzen 1970;
Connell 1971). Another possible explanation for conspecific
density dependence might be expected to be stronger in com-
munities with high population density, reaching its limit in
single species stands where self-thinning laws are applicable
(Niklas et al. 2003).
4.4 The effects of the habitat filtering on density
dependence
The role of density dependence, without considering the effect
of habitat heterogeneity, may be misinterpreted (Piao et al.
2013). Tests for community level consequences of density
dependence must account for habitat heterogeneity (Chen
et al. 2010). Without accounting for habitat heterogeneity,
conspecific thinning is likely to result from unfavorable hab-
itat and not from tree-tree interactions (Piao et al. 2013).
Habitat heterogeneity may explain more mechanisms of den-
sity dependence. Wu et al. (2016a) have shown that focal
species with habitat variables considered suffered stronger
negative density dependence effects than those without habitat
variables considered.
In our study, soil moisture was factored out. Seedling sur-
vival was most strongly impacted by the density of conspecif-
ic seedling and adult neighbors in relatively low soil moisture
habitats and weaker conspecific negative density dependence
(CNDD) in relatively high soil moisture habitats. Usually, the
activities of species- or genera-specific pathogens and other
specialized natural enemies may decrease in areas of low soil
moisture, which might also cause weaker CNDD there, an
example of habitat filtering. Such relationships are likely the
result of the effect of habitat carrying capacity; because of the
scarcity of resources (e.g., soil moisture), the competition of
conspecific individuals for shared resources should lead to
negative density dependence. Seedling-seedling competition
is strong in our forest, in contrast to some studies in tropical
25 Page 10 of 12 Annals of Forest Science (2018) 75:25
forests (Paine et al. 2008; Svenning et al. 2008; Zhu et al.
2015). For example, Lebrija-Trejos et al. (2014) discounted
direct seedling-seedling competition, because they considered
that seedling neighbors rarely have direct contact with one
another and their impacts on resource use are likely to be
slight. However, unfortunately, we could not disentangle the
activities of specialized natural enemies from intraspecific
competition given the observational nature of our analyses.
Both heterospecific seedling neighbor densities and
heterospecific adult neighbor densities positively impact on
seedling survival. Seedling survival was significantly posi-
tively impacted by herbal density at medium soil moisture
localities. These findings may provide evidence for another
theory, the “species herd protection hypothesis”(Peters 2003).
Heterospecific neighborhoods are known to result in fewer
encounters between a host and its species-specific pests and
pathogens, a condition which reduces the transmission of nat-
ural enemies and increases rates of survival (Peters 2003). The
hypothesis explicitly considered the implications of biotic in-
teractions mediated by heterospecific neighbors, which may
be seen as an extension of the Janzen-Connell hypothesis.
In our study, we found evidence of a phylogenetic positive
density dependence (PPDD) among the seedling-seedling re-
lations when soil moisture ≤42% and ≤45% (Table 4). This
result is in line with the study of Sedio et al. (2012), who found
that both hydraulic traits and species’responses to water avail-
ability were phylogenetically based, leading to phylogenetic
clustering of species within microhabitats. The effect of
seedling-seedling PPDD was enhanced with an increase in
soil moisture, which may reflect habitat preferences resulting
from habitat filtering: trees survive well and occur at higher
densities in the most suitable habitat for the species (Zhu et al.
2015). The heterogeneity of spatial resources may be masking
the signs of potential negative density dependence. It is not
only difficult to test negative density dependence in habitats
suitable for population growth, but it will also give the illusion
of a positive density dependence effect(Zhu et al. 2009). It has
also been suggested that perhaps other habitat variables or
some as-yet unrecognized mechanism may be effective (Wu
et al. 2016a,b).
5 Conclusion
In this study, we integrated effect of distance dependence,
conspecific negative density dependence (CNDD), phyloge-
netic density dependence (PNDD/PPDD), and habitat filtering
in temperate tree seedling survival. Some results were found.
(1) The strongest CNDD was found within a radius of 15 m.
(2) Seedling survival were most strongly impacted by the
density of conspecific seedling- and adult- neighbors in hab-
itats with relatively low soil moisture and less in higher mois-
ture habitats. (3) The effect of seedling-seedling CNDD was
especially significant, when densities were ranged from 20 to
40 seedlings/4 m
2
. (4) There was some evidence of phyloge-
netic positive density dependence (PPDD), and the effect of
seedling-seedling PPDD was increasing with an increase in
soil moisture. Our results demonstrate that conspecific nega-
tive density dependence played an important role in seedling
survival, which is closely related to habitat filtering and pop-
ulation density. However, we found some evidences of phy-
logenetic positive density dependence. We suggest that future
studies of neighborhood density dependence should increase
awareness of evolutionary relationships.
Data availability The datasets generated during and/or ana-
lyzed during the current study are available from the corre-
sponding author on reasonable request.
Acknowledgements We thank Jian Li and Jianghuan Qin for help with
field work, Chunyu Fan and Lingzhao Tan for helping gather relevant
literature about models with R software, and anonymous reviewers for
their constructive comments and suggestions on previous version of the
manuscript.
Funding information Funding for this research is supported by the Key
Project of National Key Research and Development Plan
(2017YFC0504005) and the Program of National Natural Science
Foundation of China (31670643).
Conflicts of interest The authors declare that they have no conflict of
interest.
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